大麦芽期耐盐相关的同源和候选基因

Salinity tolerance in barley during germination—homologs and potential genes # # 大麦芽期耐盐相关的同源和候选基因 1 2 first-author 1 2 3 1 2 1 2 3 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:c.li@murdoch.edu.au †E-mail:c.li@murdoch.edu.au c.li@murdoch.edu.au Western Barley Genetics Alliance, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA 6150, Australia Western Barley Genetics Alliance, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA 6150, Australia Western Australian State Agricultural Biotechnology Centre, Murdoch University, Murdoch, WA 6150, Australia Western Australian State Agricultural Biotechnology Centre, Murdoch University, Murdoch, WA 6150, Australia Department of Primary Industries and Regional Development, 3 Baron-Hay Court, South Perth, WA 6151, Australia Department of Primary Industries and Regional Development, 3 Baron-Hay Court, South Perth, WA 6151, Australia Salinity affects more than 6% of the world’s total land area, causing massive losses in crop yield. Salinity inhibits plant growth and development through osmotic and ionic stresses; however, some plants exhibit adaptations through osmotic regulation, exclusion, and translocation of accumulated Na + or Cl − . Currently, there are no practical, economically viable methods for managing salinity, so the best practice is to grow crops with improved tolerance. Germination is the stage in a plant’s life cycle most adversely affected by salinity. Barley, the fourth most important cereal crop in the world, has outstanding salinity tolerance, relative to other cereal crops. Here, we review the genetics of salinity tolerance in barley during germination by summarizing reported quantitative trait loci (QTLs) and functional genes. The homologs of candidate genes for salinity tolerance in Arabidopsis , soybean, maize, wheat, and rice have been blasted and mapped on the barley reference genome. The genetic diversity of three reported functional gene families for salt tolerance during barley germination, namely dehydration-responsive element-binding (DREB) protein, somatic embryogenesis receptor-like kinase and aquaporin genes, is discussed. While all three gene families show great diversity in most plant species, the DREB gene family is more diverse in barley than in wheat and rice. Further to this review, a convenient method for screening for salinity tolerance at germination is needed, and the mechanisms of action of the genes involved in salt tolerance need to be identified, validated, and transferred to commercial cultivars for field production in saline soil. 土壤盐害影响了全球6%以上的陆地面积,并导致了大量的农作物减产.盐害主要通过渗透和离子胁迫抑制植物的生长和发育,而植物相应地通过渗透调节、转移或外排积累的钠和氯离子以增强适应性.目前,生产上尚未有实用、经济的方法治理盐害,因而最为可行的途径是增强植物自身的耐盐性.盐胁迫严重抑制种子萌发,而作为全球第四大禾谷类作物的大麦与其他谷物相比耐盐性更强.本文综述了大麦芽期耐盐性的遗传机制,总结了已报道的相关数量性状位点和功能基因,比对了拟南芥、大豆、玉米、小麦和水稻中耐盐候选基因在大麦中的同源基因并映射到参考基因组.此外,本文还讨论了三个耐盐功能基因家族的遗传多样性,包括脱水应答元件结合蛋白(DREB)、类体细胞胚胎发生受体激酶和水通道蛋白.上述三个基因家族在植物中都存在丰富的多样性,但DREB家族在大麦中的多样性高于水稻和小麦.后续研究中,芽期耐盐性的简便筛选方法仍有待开发,耐盐基因及相关机理机制仍需鉴定、验证,并整合到栽培品种中,以实现盐土上作物的生产. Genetics Barley Quantitative trait locus (QTL) Germination Salinity tolerance Homologous gene Diversity 遗传 大麦 数量性状位点 发芽 耐盐性 同源基因 多样性 Introduction 1 Salinity affects about 6% of the world’s total land area, including 20% of arable land and 33% of irrigated land (Shrivastava and Kumar, 2015 2015 ; Machado and Serralheiro, 2017 2017 ; Kuang et al., 2019 2019 ; Safdar et al., 2019 2019 ), causing estimated yield losses of 20% (Ashraf and Harris, 2005 2005 ; Pirasteh-Anosheh et al., 2016 2016 ). Furthermore, land salinisation is increasing, with 10 million ha of agricultural land destroyed annually by salt accumulation (Pimentel et al., 2004 2004 ) due to several factors including the use of contaminated irrigation water, intensive farming and poor drainage, and climate change (Machado and Serralheiro, 2017 2017 ; Isayenkov, 2019 2019 ). Without proper and sustainable control, salinity-affected areas will increase to more than 50% of the world’s total arable land by 2050 (Ashraf, 2009 2009 ; Anosheh et al., 2011 2011 ; Jamil et al., 2011 2011 ; Emam et al., 2013 2013 ). According to Pirasteh-Anosheh et al. ( 2016 2016 ), plants experience four types of stress under saline conditions: (1) salinity reduces water uptake due to the low water potential of the soil which interferes with the osmotic gradient (Munns and Tester, 2008 2008 ); (2) the absorbed salt reaches a level that causes severe cellular toxicity due to low sequestration of Na + into vacuoles (Nawaz, 2007 2007 ); (3) the salt interacts with minerals causing nutrient imbalance and deficiency (Nawaz, 2007 2007 ); and (4) salinity accelerates the production of active oxygen radicles, such as H 2 O 2 (hydrogen peroxide), •O 2 − (superoxide), ¹O 2 (singlet oxygen), and •OH − (hydroxyl radicle), which can damage or even kill plants (Hernández et al., 2001 2001 ). Greenway and Munns ( 1980 1980 ) classified plants into two major categories based on their salinity tolerance, namely (1) halophytes and (2) glycophytes. Halophytes have an exceptional ability to produce heteromorphic seeds that have diverse dormancy and germination capacity under saline conditions (Liu RR et al., 2018 2018 ). Seed germination in glycophytes is severely inhibited under salinity due to both osmotic stress and ionic toxicity stress, unlike in halophytes that are less affected by osmotic pressure (Romo and Haferkamp, 1987 1987 ; Dodd and Donovan, 1999 1999 ; Zhang et al., 2010 2010 ). Halophytes can better regulate the ion-gate-controlled NaCl influx into seed cells (Glenn et al., 1999 1999 ; Huang et al., 2018 2018 ). However, salinity-tolerant glycophytes have a lower osmotic potential than sensitive glycophytes, enabling them to absorb more water from the soil during germination (Zhang et al., 2010 2010 ). Barley, the fourth most important cereal in the world (Schulte et al., 2009 2009 ; Visioni et al., 2019 2019 ), is a glycophyte, but its salinity tolerance varies among genotypes (Mano and Takeda, 1997 1997 ; Flowers and Hajibagheri, 2001 2001 ; Xue et al., 2009 2009 ; Debez et al., 2019 2019 ). Some barley genotypes are able to thrive in saline conditions (Harlan, 1995 1995 ; Shen et al., 2018 2018 ). Salinity-tolerant barley genotypes exhibit halophytic features such as excluding Na + from uptake (Chen ZH et al., 2007 2007 ) and accumulating Na + in tissues (Munns et al., 1988 1988 ; Munns and Tester, 2008 2008 ). Tolerant genotypes sequester Na + in their intracellular vacuoles, thereby maintaining high K + /Na + levels in the cytosol while reducing damage from Na + toxicity (Shabala et al., 2010 2010 ; Mian et al., 2011 2011 ; Fu et al., 2018 2018 ; Han et al., 2018 2018 ; Ishikawa and Shabala, 2019 2019 ). They can also synthesize compatible solutes in the cytoplasm to balance the osmotic potential of vacuolar Na + (Widodo et al., 2009 2009 ). Salinity tolerance is controlled by multiple genes that are expressed differently during different growth phases (Qiu et al., 2011 2011 ; Ahmed et al., 2013a 2013a ). Germination, which determines seedling vigour and the plant population, is the most important growth stage, but is sensitive to salinity stress (Zhang et al., 2010 2010 ; Bewley et al., 2013 2013 ). Several genes have association with enhanced salinity tolerance in barley (Wu et al., 2011 2011 ) and are grouped into four classes based on their function (Walia et al., 2006 2006 ; Wu et al., 2011 2011 ; Yin et al., 2018 2018 ). (1) Genes that enhance osmotic protection, such as HvPIP2;5 (Alavilli et al., 2016 2016 ), HVA1 (Lal et al., 2008 2008 ), HvDREB1 , HvCBF4 , HvWRKY38 (Gürel et al., 2016 2016 ), and reactive oxygen species (ROS)-scavenging genes that include osmoregulatory trehalose synthesis, mannitol-1-phosphate dehydrogenase (M1PD), and pyrroline-5-carboxylase synthetase (P5CS). (2) Genes controlling Na + and K + transport, such as the high-affinity potassium transporter ( HKT ) family (e.g. HvHKT1;5 (Hazzouri et al., 2018 2018 ; Huang et al., 2019 2019 ), HvHKT1;1 (Han et al., 2018 2018 ), HvHKT2;1 (Mian et al., 2011 2011 ; Assaha et al., 2017 2017 ), HvHAK1 (Mangano et al., 2008 2008 ), HvHKT1 , HvHKT2 (Qiu et al., 2011 2011 )), the Na + /H + exchanger ( NHX ) family ( HvNax4 (Rivandi et al., 2011 2011 ), and salt overly sensitive (SOS) engaged Na + /H + antiporters ( HvSOS1 ( HvNHX7 ), HvSOS2 ( HvCIPK24 ), HvSOS3 ( HvCBL4 ), HvNHX1 , HVA ) (Yousefirad et al., 2018 2018 ; Wu et al., 2019 2019 ). (3) Genes that produce regulatory proteins, such as the CBF / DREB (C-repeat-binding protein/dehydration-responsive element-binding protein) family (e.g. HvRAF (Jung et al., 2007 2007 ), HvAP2 / ERF (ethylene response factor) (Guo et al., 2016 2016 ), HvDREB1 (Xu et al., 2009 2009 ), HvCBF4 , HvWRKY38 (Gürel et al., 2016 2016 ), HvDRF1 (Xue and Loveridge, 2004 2004 )) in the signalling pathways of long distance and downstream gene expression. Salinity and drought stresses induce the expression of root abundant factor ( RAF ), CBF3 , and CBF4 from the CBF / DREB gene family in most plants. Twenty CBF genes have been identified in barley, which enhance tolerance to drought, salinity, and low temperature (Wu et al., 2011 2011 ). (4) Genes that induce jasmonate (JA) biosynthesis, such as late embryogenesis abundant (LEA) protein genes (e.g. HVA1 expressed in response to water and salinity stresses, HVA22 expressed in response to dehydration, extreme temperatures, abscisic acid (ABA) secretion, and salinity stress (al-Yassin and Khademian, 2015 2015 )). Seed germination process and roles of hormones 1 Seed germination requires optimum environmental factors, including water, oxygen, and temperature. Other environmental factors, such as light and nitrates, can also affect seed germination (Finch-Savage and Leubner-Metzger, 2006 2006 ; Rajjou et al., 2012 2012 ). The process of germination occurs in three main phases regulated by hormones, reactive nitrogen species, and ROS (Ma et al., 2017 2017 ). The first phase involves the expression of genes that play a major role in cell wall metabolism. The second phase encompasses significant stimulation of hormonal and enzyme activity by genes involved in amino acid synthesis, starch metabolism, nucleic acid synthesis, protein synthesis and transport (Weitbrecht et al., 2011 2011 ). The third phase involves the induction of genes for photosynthetic metabolism after radicle protrusion (Ma et al., 2017 2017 ). Hormonal imbalance, caused by factors such as low temperature, drought, and salts (saline and sodic) that increase ground osmotic pressure (Bartels and Nelson, 1994 1994 ), can affect the seed germination process (Lopez-Molina et al., 2001 2001 ; Belin and Lopez-Molina, 2008 2008 ). Several hormones produced by plant and soil microorganisms such as bacteria play a role in inducing or breaking seed dormancy and thus contribute to the germination process (Bewley, 1997 1997 ; Baskin and Baskin, 2001 2001 ; Koornneef et al., 2002 2002 ; Hoyle et al., 2015 2015 ). Interestingly, as much as gene expression controls plant hormone activity, the reverse can be true with some hormones regulating gene expression (Miransari and Smith, 2014 2014 ). For example, ABA usually induces dormancy at seed maturation and gibberellins (GAs) break dormancy during germination (Fig. 1 1 ) (Bentsink and Koornneef, 2008 2008 ; Hauvermale et al., 2012 2012 ). When an environmental stress such as salinity occurs during germination, ABA is produced in the seeds (Weyers and Paterson, 2001 2001 ) to upregulate transcription factors (TFs) such as AB13 and AB15 that stimulate genes encoding the osmotolerance protein and block the germination process (Fedoroff, 2002 2002 ; Lopez-Molina et al., 2002 2002 ; Graeber et al., 2010 2010 ; Miransari and Smith, 2014 2014 ). However, ABA is negatively regulated by ABA-INSENSITIVE1 ( ABI1 ) and ABI2 and the expression of the HvABA8′OH-1 gene (Ma et al., 2017 2017 ). GAs release seeds from dormancy by stimulating the production of hydrolases for the germination process (Miransari and Smith, 2014 2014 ; Abido et al., 2019 2019 ). The embryo synthesizes GA after imbibing water (Diaz-Mendoza et al., 2019 2019 ). The GA binds to receptors to promote the breakdown of repressor of GA-like2 (RGL2), a DELL factor suppressing germination, the expression of several genes ( GAMYB , HvPTR , WRKY , PP2C , GATA , and HvKAO1 ), and the production of essential proteins during germination in stress environments (Marrs, 1996 1996 ; Sun and Gubler, 2004 2004 ; Ma et al., 2017 2017 ). The effect of GA is terminated by the expression of GA 2-oxidase 1 ( HvGA2ox ), which is responsible for its inactivation (Fig. 1 1 ) (Ma et al., 2017 2017 ). Blue lines indicate hormonal regulation, while black lines are for genes and transcription factor expression. Red double-arrowed dotted line shows the negative interaction between ABA and GA during germination, while blue double-arrowed line shows the positive interaction among the hormones. Blue dotted lines show the stimulation outcome of the hormonal interactions, while black dotted lines show the regulatory interactions of genes. GAMYB : GA-induced Myb (myeloblastosis)-like protein; HvPTR : barley scutellar peptide transporter; HvKAO1 : barley kaurenoic acid oxidase 1; HvGA2ox : barley GA 2-oxidase 1; HvNCED : barley nine- cis -epoxycarotenoid dioxygenase; PP2C : protein phosphatase type 2C; ABI1 : ABA-insensitive 1; HvABA8′OH-1 : barley ABA 8' hydroxylase; HvCBL : barley calcineurin B-like protein; HvSERK : barley somatic embryogenesis receptor-like kinase; HvCBF : barley C-repeat-binding protein; HvDREB : barley dehydration-responsive element-binding protein; HvRAF : barley root abundant factor; HvPIP2;5 : barley aquaporin 2;5 During germination, the concentration of ethylene increases (Yang and Hoffman, 1984 1984 ; Pennazio and Roggero, 1991 1991 ; Petruzzelli et al., 2000 2000 ), which reduces plant growth under saline conditions in the presence of ABA (Matilla, 2000 2000 ; Rinaldi, 2000 2000 ; Jalili et al., 2009 2009 ). Auxins (indole-3-acetic acids (IAAs)) are essential for cell elongation, and radicle and embryo growth during germination (Popko et al., 2010 2010 ; Hauvermale et al., 2012 2012 ). Brassinosteroids (BRs) and IAA on the other hand stimulate the secretion of ethylene which works in conjunction with GAs to induce germination (Arora, 2005 2005 ; Miransari and Smith, 2014 2014 ). Auxins reduce seed sensitivity to ABA by overexpressing microRNAs (Liu et al., 2007 2007 ) and interacting with GAs to counteract ABA suppression during germination (Chiwocha et al., 2005 2005 ; Hentrich et al., 2013 2013 ). Cytokinins interacting with ethylene enhance cell division and alleviate abiotic stresses like salinity during germination (Chiwocha et al., 2005 2005 ; Subbiah and Reddy, 2010 2010 ; Peleg and Blumwald, 2011 2011 ; Miransari and Smith, 2014 2014 ). BRs, in conjunction with GAs and ethylene, improve seed resistance to abiotic stress, enhance embryo growth out of the seed, and reduce the effects of ABA (Bajguz and Hayat, 2009 2009 ; Miransari and Smith, 2014 2014 ; Procházka et al., 2015 2015 ) and salt stress (Vázquez et al., 2019 2019 ) during germination. JAs are signalling molecules for plant defence against osmotic stress caused by salt (Kazan and Manners, 2012 2012 ; Nguyen et al., 2019 2019 ). They obstruct the production of two primary ABA biosynthesis genes ( TaNCED1 and TaNCED2 ) with acetylsalicylic acid (ASA) in stress germination in wheat (Xu et al., 2016 2016 ). Salinity versus sodicity 1 Saline soils predominantly contain sodium (Na + ) cations and chloride (Cl − ) anions and, in some cases, Ca 2+ , Mg 2+ , SO 4 2− , but not HCO 3 − or CO 3 2− (Abrol et al., 1988 1988 ). Saline soils have good structure, an advantage for proper tillage and crop cultivation, and usually an electric conductivity extract (ECE) higher than 4 dS/m (40 mmol/L), an exchangeable water-soluble sodium of > 15%, and a pH of < 8.5 but > 7. However, when the surface of the ground appears black, hard, and dry, the soil is sodic. In this case, the predominant cation is Na + , but the primary anions are Cl − , SO 4 2− , HCO 3 − and a small amount of CO 3 2− . Sodic soils have an exchangeable Na + of > 15%, an ECE of > 4 dS/m, and a pH of > 8.5 (Abrol et al., 1988 1988 ). Causes and types of salinity 2 Soil salinity is caused by (1) natural or primary, and (2) secondary or human-induced events (Manchanda and Garg, 2008 2008 ; Parihar et al., 2015 2015 ) and is either (1) groundwater-associated (dryland salinity), (2) non-groundwater-associated (transient salinity), or (3) irrigation-associated (Ghassemi et al., 1995 1995 ; Rengasamy, 2006 2006 ; Majeed and Muhammad, 2019 2019 ). Transient salinity fluctuates with soil depth and its effect on plant growth is dependent on rainfall. It occurs in semi-arid environments where there is insufficient rain to leach the soil. Clay layers below the topsoil hinder the movement of water and salts, leading to ion accumulation on the soil surface (Rengasamy, 2002 2002 , 2006 2006 ). Most of Western Australia is characterized by a temperate climate. Ion accumulation in the topsoil following dry, hot summers can result in high salinity at sowing, which affects seed germination. These ions can be leached only by rainfall or irrigation. Dry-seeding or seeding with the first rain increases the likelihood that germinating seeds will be affected by salinity stress. Effect of salinity on germination 2 Salinity affects the seed germination process by altering water imbibition, changing enzymatic activities causing ionic toxicity, interfering with protein metabolism, causing hormonal imbalances, and reducing the possibility of seeds using their reserves, all of which delay and reduce the number of sprouting seeds (Läuchli and Grattan, 2007 2007 ; Bordi, 2010 2010 ; Munns et al., 2012 2012 ; Parihar et al., 2015 2015 ; Debez et al., 2019 2019 ). Saline conditions create an external osmotic stress that reduces water availability and uptake (Bernstein, 1963 1963 ; Bliss et al., 1986 1986 ; Sayar et al., 2010 2010 ; Sabagh et al., 2019 2019 ) and increases the toxic absorption of ions (Hampson and Simpson, 1990 1990 ), which decreases seed germination (Dodd and Donovan, 1999 1999 ; Luan et al., 2014 2014 ; Narsing Rao et al., 2019 2019 ; Polash et al., 2019 2019 ). Salinity tolerance mechanisms 2 Plants overcome salinity stress through various mechanisms that involve osmotic adjustment, Na + exclusion, and tissue tolerance (Munns and Tester, 2008 2008 ; Liang et al., 2018 2018 ; Miransari and Smith, 2019 2019 ). These encompass biochemical, physiological, and molecular mechanisms of variable complexity (Han et al., 2015 2015 ; Pirasteh-Anosheh et al., 2016 2016 ; Kumari et al., 2019 2019 ). During germination, plants become saline-tolerant by (1) excluding salts from seed cells while maintaining high osmotic potential using organic solutes, or (2) accumulating salt ions in seed cells to increase osmotic potential while putting mechanisms in place to mitigate toxicity (Zhang et al., 2010 2010 ). Seeds of salt-tolerant barley genotypes take up sodium to increase osmotic potential to absorb water during germination under salinity stress (Zhang et al., 2010 2010 ), while minimising K + losses (al-Karaki, 2001 2001 ). The vacuole is a vital cell organelle for compound deposition during osmotic stress regulation, and its size is a measure of salinity tolerance (Lauchli and Epstein, 1990 1990 ; Volkmar et al., 1998 1998 ; Yarra, 2019 2019 ; Yarra and Kirti, 2019 2019 ). 3.3.1 Indicators of salinity tolerance Salinity tolerance indicators in plants can be divided into three main groups: (1) agronomic/morphological, (2) physiological, and (3) biochemical. 3.3.1.1 Agronomic/morphological indicators Salinity tolerance is expressed externally through visible morphological/agronomic traits as a result of several physio-chemical processes that take place inside the plant. They are a reflection of genetic and physiological mechanisms influenced by the environmental effect on the plant that confer salinity tolerance (Ashraf and Harris, 2004 2004 ). They occur at the whole plant or organ level and are mostly physically visible. These indicators are easy to measure and include germination percentage, yield, survival rate/percentage, plant height, leaf area, leaf injury, relative growth rate, and relative growth reduction. Distinguishing between tolerant and non-tolerant plants using agronomic indicators can be subjective. 3.3.1.2 Physiological indicators Like the other indicator groups, physiological indicators are the result of processes that take place inside plant tissues, organs, cells, and organelles when exposed to salinity stress. They include the transportation of excess ions to the vacuole or sequestering them in older tissues. This group of indicators is measured by traits that include relative growth rate, germination speed, ion homeostasis, photosynthesis, transpiration, and senescence (Negrão et al., 2017 2017 ). They provide more objective information than morphological indicators when combined with knowledge of the genetic model of salinity tolerance (Ashraf and Harris, 2004 2004 ). Sodium ions are transported and compartmentalized in the vacuoles using two types of H + pumps (V-ATPase and H + -ATPase) and vacuolar pyrophosphatase (V-PPase). The pumps are facilitated by SOS pathways with three types of proteins (SOS 1 , SOS 2 , and SOS 3 ). SOS 1 is essential for regulating Na + efflux at the cellular level and enhancing Na + transportation in the organelles and tissues. The SOS 2 can not only interact with SOS 3 and subsequently activate SOS1, but also increases transport activity of proteins such as NHX (Gupta and Huang, 2014 2014 ). Electron transport chains in mitochondria can overflow, deregulate, or become disrupted by salinity stress leading to the accumulation of toxic compounds. Antioxidant enzymes and nonenzymatic compounds are essential for detoxifying ROS, which include helicase proteins, catalase (CAT), peroxidase, polyphenol, flavonoid, ascorbate, and glutathione (Gupta and Huang, 2014 2014 ). 3.3.1.3 Biochemical indicators Biochemical indicators are chemical solutes that build up inside plants in response to salt stress (Ashraf and Harris, 2004 2004 ). The accumulation of low molecular weight organic solutes, inorganic ions, compatible osmolytes, soluble sugars, soluble proteins, amino acids and amides, quaternary ammonium compounds, polyamines (PAs), polyols, antioxidants, and ATPases is associated with tolerance to salinity stress. Secretion of biochemical compounds occurs during healthy growth and germination; hence it is not easy to tell whether a chemical is a reaction or tolerance to salinity stress, or an adaptive plant mechanism (Ashraf and Harris, 2004 2004 ). Plant compatible osmolytes are organic compounds synthesized by various plant species which accumulate in variable amounts and are soluble in cells and do not disturb cellular activities at high or low concentrations (Hanin et al., 2016 2016 ). These compounds, including proline, glycine betaine, sugars, and polyols, increase within the cell in response to salinity stress, and are sustained by permanent synthesis and/or degradation. Accumulation of these compounds is proportional to the surrounding osmolarity, and they function to shield the cell structure and maintain osmotic balance through constant water entry (Hasegawa et al., 2000 2000 ; Mansour and Ali, 2017 2017 ; Alhasnawi, 2019 2019 ). The secretion of PAs has a diverse function in healthy plant growth, including seed germination, and is critical for abiotic stress adaptation, including salinity. Diamine putrescine (PUT), tetra-amine spermine (SPM), and triamine spermidine (SPD) are some typical PAs found in plants (Shu et al., 2012 2012 ) and whose increase has been associated with salinity stress (Gupta and Huang, 2014 2014 ). Nitric oxide (NO) regulates several plant growth and developmental activities, stress signalling molecules and stress responses, including salinity and the activation of antioxidant enzymes (superoxide dismutase (SOD), CAT, guaiacol peroxidase (GPX), ascorbate peroxidase (APX), and glutathione reductase (GR)), and triggers the expression of various redox-regulated genes that enhance germination and root growth under salinity stress (Gupta and Huang, 2014 2014 ). Salinity stress mitigation by NO is due to its antioxidant functions, modulation of the ROS detoxification system (Mishra et al., 2011 2011 ) associated with an increase in antioxidant enzymes, such as SOD, CAT, GPX, APX, and GR (Zhao et al., 2004 2004 ; Ali et al., 2018 2018 ), and suppression of malondialdehyde (MDA) production during lipid peroxidation (Nalousi et al., 2012 2012 ). NO offers a force for Na + /H + exchange, providing the H + gradient to stimulate H + -ATPase (H + -PPase) and contributing to K + and Na + homeostasis (Zhang et al., 2006 2006 ; Gupta and Huang, 2014 2014 ). Other biochemical indicators include the production of several hormones in response to salinity stress, including ABA in roots and shoots, which mitigates the antagonistic effect of salinity stress on physiological processes (Popova et al., 1995 1995 ; Jaschke et al., 1997 1997 ). ABA accumulation triggers the expression of salinity stress tolerance enhancing genes in cultivated barley ( HVP1 , HVP10 , and HvVHA-A ) and wheat ( MAPK4-like , TIP 1 , and GLP 1 ) (Keskin et al., 2010 2010 ). Salicylic acid (SA) concentration, along with the SA biosynthetic enzyme, increases under salinity stress in rice seedlings (Jayakannan et al., 2013 2013 ). Application of BR promotes antioxidant enzyme (SOD, POX, APX, and GPX) activity and the accumulation of salinity stress mitigating nonenzymatic antioxidant compounds, such as tocopherol, ascorbate, and reduced glutathione (Ashraf et al., 2010 2010 ; el-Mashad and Mohamed, 2012 2012 ; Gupta and Huang, 2014 2014 ). 3.3.2 Salinity stress signalling pathways and molecules The response to salinity stress in plants involves three types of signalling pathway: (1) ionic and osmotic stress signalling (homeostasis) essential for the re-establishment of cellular homeostasis, (2) detoxification signalling that regulates and repairs damage, and (3) cell division and expansion signalling (Zhu, 2001 2001 ). Homeostatic signalling governs detoxification leading to tolerance by reducing the response of growth inhibitors (Zhu, 2002 2002 ). The signalling information flows in a way that ionic (Na + ), osmotic (turgor pressure change), and detoxification are stress input, while salinity-induced damage, control, and repair are output (response) (Xiong and Zhu, 2001 2001 ; Zhu, 2002 2002 ). The outcomes of osmotic signalling include gene expression or activation of osmolyte biosynthesis enzymes and the water and osmolyte transport system (Zhu, 2001 2001 ). Detoxification signalling changes induced by salt include phospholipid hydrolysis, changes in the expression of LEA/dehydrin-type genes, molecular chaperones, and proteinase to remove denatured proteins, and the activation of enzymes for the generation and removal of ROS and other detoxification proteins (Zhu, 2001 2001 , 2002 2002 ). Signalling molecules are crucial components for salinity stress tolerance in plants, and they determine downstream actions involving protein phosphorylation, dephosphorylation, phospholipid metabolism, and calcium ion (Ca 2+ ) sensing (Agarwal et al., 2013 2013 ). Ca 2+ signalling is one of the first responses to salt stress and is essential for ion homeostasis (Zhu, 2003 2003 ; Reddy and Reddy, 2004 2004 ). It is sensed by calcineurin B-like proteins (CBLs) that are involved in the salt stress indication transduction pathway and govern the influx and efflux of Na + . CBLs increase germination under salinity stress in tobacco (Pardo et al., 1998 1998 ), Arabidopsis (Liu and Zhu, 1998 1998 ), and maize (Wang MY et al., 2007 2007 ). Other molecules include mitogen-activated protein kinase (SAPK) (Diédhiou et al., 2008 2008 ), CBL-interacting protein kinase (CIPK), nucleoside diphosphate kinase (NDPK), and mitogen-activated protein (MAP) kinase (MPK) (Moon et al., 2003 2003 ), whose overexpression enhances salinity tolerance capacity by increasing seed germination. Initiation of the MPK cascade is the second response to decode external salinity stress into cellular responses (Teige et al., 2004 2004 ). This includes signalling modules that phosphorylate particular serine/threonine residues on amide protein substrates that regulate several cellular processes (MAPK Group et al., 2002 2002 ). Overexpression of MAP in rice (Xiong and Yang, 2003 2003 ; Jeong et al., 2006 2006 ) and maize MAP in Arabidopsis (Kong et al., 2011 2011 ) enhances salinity tolerance and activates transcriptional factors controlling downstream genes such as COR47 , RD29A , P5CS2 (Wurzinger et al., 2011 2011 ), and CDPK (Capiati et al., 2006 2006 ). 3.3.3 Salinity stress tolerance: transcriptional regulation and gene expression Salt stress prompts the induction of various genes that fall into two broad groups: (1) single function genes that facilitate the production of protective metabolites, and (2) regulatory genes that control the expression of downstream genes (Agarwal et al., 2013 2013 ). Single function genes promote the release of compounds such as transporters/channel proteins, osmolytes, lipid biosynthesis genes, antioxidative enzymes, and PAs, while DREB , bZIP , NAC , and MYC/MYB (myelocytomatosis/myeloblastosis) are regulatory genes (Shinozaki and Yamaguchi-Shinozaki, 2007 2007 ; Agarwal and Jha, 2010 2010 ). Many of these genes from both groups play different roles in enhancing the adaptation process, and are further categorized into functional groups that include: (1) senescence-associated genes (SAGs), (2) ion transport or homeostasis genes ( SOS , HKT , AtNHX1 , and H + -ATPase ), (3) molecular chaperones ( HSP genes), and (4) dehydration-related TFs ( DREB ) (Hasegawa et al., 2000 2000 ; Liu et al., 2000 2000 ; Shi et al., 2000 2000 ; Yen et al., 2000 2000 ). Under osmotic pressure from salinity stress, plants synthesize novel proteins that increase the expression of genes, such as osmotic regulation (OR) genes, at the cell level to aid their adaptation. The OR genes are categorized into nine groups, namely LEA genes, osmolyte biosynthesis genes, transporter genes, OR genes that encode regulatory proteins, photosynthetic genes, OR genes encoding proteins involved in protein synthesis processes and degradation, heat shock protein genes, osmotins, and other protein genes (Zhu et al., 1997 1997 ; Turan et al., 2012 2012 ). Other OR genes include those encoding RNA-binding proteins, putative lipid transfer, RD29A , RD29B , Kin1 , and Kin2 . Considerable variation among factors such as plant tissue type, age, and developmental stage also affects the expression of OR genes (Zhu et al., 1997 1997 ). Transcription factors (TFs), including bZIP , WRKY , AP2 , NAC , C 2 H 2 zinc finger gene, and DREB , are the most important regulators of gene expression under salinity stress (Gupta and Huang, 2014 2014 ). They interact with diverse cis -elements in the promoter regions of many downstream genes and modify their expression. There are many different types of TFs in the plant kingdom (Shiu et al., 2005 2005 ) with more than 50 families distinguished by their DNA-binding domains (Riechmann et al., 2000 2000 ). Several TFs have been identified in Arabidopsis , including a basic-leucine zipper, AP2/ERF (APETALA2/ethylene-responsive factor), MYC , HD-ZIP (homeodomain-leucine zipper ) , MYB , and different classes of zinc finger domains (Shinozaki and Yamaguchi-Shinozaki, 2000 2000 ). The expression of a given number of genes occurs through TF interactions with non-DNA-binding proteins and/or cis -regulatory elements (Grotewold, 2008 2008 ). On the same transduction pathways, ABA, SA, ethylene, BR, and JA regulate TF expression (Agarwal et al., 2006 2006 ; Seo et al., 2008 2008 ; Agarwal and Jha, 2010 2010 ; Gürel et al., 2016 2016 ). The four classes of TFs are: (1) ABA-dependent (CBF/DREB proteins), (2) ABA-independent (MYC, MYB, ABA-responsive element-binding protein (AREB), ABA-binding factor protein (ABF)) (Agarwal and Jha, 2010 2010 ; Liu SW et al., 2018 2018 ), (3) ABA-dependent and -independent (no apical meristem, ATAF1,2 and cup-shaped cotyledon (NAC)) (Agarwal et al., 2013 2013 ; Joshi et al., 2016 2016 ), and (4) TFs that do not belong to any of the first three groups, including homeodomain TFs osmotically responsive gene 9 (HOS9) and an R2R3-type MYB protein (HOS10) (Zhu et al., 2004 2004 , 2005 2005 ). Genetics of salinity tolerance at germination in barley 1 QTLs for salinity tolerance in barley and the homologous genes from Arabidopsis , soybean, maize, wheat, and rice at the germination stage 2 At the germination stage, salinity tolerance is controlled by various loci (Mano and Takeda, 1997 1997 ), indicating that it is polygenic. Angessa et al. ( 2017 2017 ) reported transgressive phenotypic segregation for germination percentage in a doubled haploid (DH) population developed from salinity-tolerant genotype CM72 and the sensitive commercial Australian barley cultivar Gairdner. Using 150 and 300 mmol/L NaCl, Angessa et al. ( 2017 2017 ) mapped two stable quantitative trait loci (QTLs) to chromosome 2H, close to the sodium concentration QTL reported by Xue et al. ( 2009 2009 ). A third QTL reported by Angessa et al. ( 2017 2017 ) at 300 mmol/L NaCl was mapped to chromosome 5H, but slightly distant from the potassium concentration-linked QTL of Xue et al. ( 2009 2009 ). Mano and Takeda ( 1997 1997 ) reported QTLs controlling ABA response on chromosomes 2H, 3H, 1H, and 5H in Steptoe/Morex DH lines, and 2H and 5H in Harrington/TR306 DH lines. In both crosses, chromosome 5H was very close to the position of the salinity tolerance QTL. A QTL analysis of the Oregon Wolf Barley mapping population (DOM×REC) by Witzel et al. ( 2010 2010 ) at the germination stage identified two chromosomal regions on 5H, one on 7H, and one on 2H associated with the salt stress response. A single chromosomal region on 5H, responsible for 42% of the variation in the phenotype, was constant across all NaCl concentrations (Table 1 1 ). 1%=0.01 g/mL Trait at germination Salt level Mapping population Analysis type QTL number and location Percentage explained Reference 3 Germination percentage 150 mmol/L NaCl 103-DH of CM72/Gairdner Bi-Parent 1 (2H) 21.8 Angessa et al., 2017 2017 300 mmol/L NaCl 103-DH of CM72/Gairdner Bi-Parent 1 (2H) 16.1 Angessa et al., 2017 2017 300 mmol/L NaCl 103-DH of CM72/Gairdner Bi-Parent 1 (5H) 10.0 Angessa et al., 2017 2017 2 Germination speed 250 mmol/L NaCl 149-DH of Steptoe/Morex Bi-Parent 2 (2H), 3 (3H), and 7 (5H) 7.6–20.3 Mano and Takeda, 1997 1997 300 mmol/L NaCl 146-DH of Harrington/TR306 Bi-Parent 1 (7H), 6 (6H), and 7 (5H) 8.7–15.3 Mano and Takeda, 1997 1997 7 Salt tolerance 250 mmol/L NaCl 149-DH of Steptoe/Morex Bi-Parent 4 (4H), 6 (6H), and 7 (5H) 6.8–46.7 Mano and Takeda, 1997 1997 300 mmol/L NaCl 146-DH of Harrington/TR306 Bi-Parent 5 (1H) and 7 (5H) 17.4–41.1 Mano and Takeda, 1997 1997 1.5% * * 94-DH of DOM/REC Bi-Parent 1 (5H) and 1 (7H) 42 Witzel et al., 2010 2010 2.0% 94-DH of DOM/REC Bi-Parent 1 (5H) and 1 (7H) 42 Witzel et al., 2010 2010 2.5% 94-DH of DOM/REC Bi-Parent 1 (5H) and 1 (7H) Witzel et al., 2010 2010 1.5% 94-DH of DOM/REC Bi-Parent 1 (2H) Witzel et al., 2010 2010 1.5%–2.5% 94-DH of DOM/REC Bi-Parent 2 (5H), 1 (7H), and 1 (2H) Witzel et al., 2010 2010 Protein sequences of functional salinity tolerance genes during germination in Arabidopsis , soybean, maize, wheat, and rice were extracted from the National Center for Biotechnology Information (NCBI) website (https:// www.ncbi.nlm.nih.gov/protein www.ncbi.nlm.nih.gov/protein ) (Benson et al., 2013 2013 ). The protein sequences in FAST formats were blasted on BARLEX (https://apex.ipk-gatersleben.de/apex/f?p=284:10) to identify homologous genes from the barley genome with the highest percentage match depending on length and expression levels in tissues at different growth stages (Colmsee et al., 2015 2015 ). There were 63 functionally characterized genes ( Arabidopsis (13), maize (4), rice (12), soybean (7), and wheat (27)) for salinity tolerance at the germination stage (Table 2 2 ). Overall, 65 homolog genes were identified in barley, with the percentage match ranging from 100% (between wheat gene TaPLDα (phospholipase D) and barley homolog gene HORVU 1Hr1G048970.4 (phospholipase D P2)) to 30% (between rice gene OsOPT10 (oligopeptide transporter family homolog) and barley’s HORVU6Hr1G067430.2 (oligopeptide transporter 4)) (Table 2 2 ). Generally, the wheat genes had the highest match with barley homologs, averaging 90.93%, followed by maize (83.00%), rice (67.58%), soybean (59.43%), and Arabidopsis (57.94%). Apart from homolog connections, gene expression patterns in tissues can suggest the function of particular genes. For instance, the expression levels of the 65 barley homologs for the first three development stages (4-d embryo (EMB), root from seedlings (ROO1; 10 cm shoot stage), and shoot from seedling stage (LEA; 10 cm shoot stage)) were more than zero for all except HORVU1Hr 1G080820.6 (CBL protein 8). The aquaporin-like superfamily protein (HORVU2Hr1G096360.13) had the highest expression levels in the EMB, ROO1, and LEA stages at 1305.90, 1094.39, and 1133.08 fragments per million kb, respectively (Table S1 S1 ) (The International Barley Genome Sequencing Consortium, 2012 2012 ; Colmsee et al., 2015 2015 ; Mascher et al., 2017 2017 ). RING, really interesting new gene; MYB, myeloblastosis; NAC, no apical meristem, ATAF1,2 and cup-shaped cotyledon; NSD, nuclear receptor-binding SET domain 2 Gene source 2 Gene ID Transgenic 2 Homolog ID in barley 2 Similarity (%) 2 Gene name in barley 2 Chromosome 2 Location 2 Reference host Arabidopsis 2 AtRZFP 2 Arabidopsis 2 HORVU5Hr1G001400.5 2 52 2 RING finger protein 5 2 5 2 4 181 876–4 184 642 2 Zang et al., 2016 2016 thaliana L A. thaliana L HORVU4Hr1G003600.1 51 RING finger protein 5 4 7 870 080–7 872 190 A. thaliana L AtNHX1 Maize/wheat HORVU2Hr1G021020.4 69 Sodium hydrogen exchanger 2 2 59 025 629–59 030 226 Yin et al., 2004 2004 ; Xue et al., 2004 2004 A. thaliana L HORVU4Hr1G033760.1 69 Sodium hydrogen exchanger 2 4 238 472 323–238 482 634 A. thaliana L HORVU7Hr1G046030.1 62 Sodium hydrogen exchanger 3 7 148 709 554–148 713 307 A. thaliana L AtSOS1 Arabidopsis HORVU3Hr1G003150.1 58 Sodium/hydrogen exchanger 7 3 8 165 119–8 185 196 Wang X et al., 2007 2007 A. thaliana L AtMYBL Arabidopsis HORVU5Hr1G077100.1 56 MYB domain protein 3R-3 5 552 718 664–552 726 337 Zhang et al., 2011 2011 2 A. thaliana L 2 RAP2.6L 2 Arabidopsis 2 HORVU2Hr1G071270.4 2 60 Ethylene-responsive 2 2 2 507 785 971–507 787 466 Krishnaswamy transcription factor 1 et al., 2011 2 A. thaliana L 2 AtERF96 2 Arabidopsis 2 HORVU4Hr1G000960.1 2 59 Ethylene-responsive 2 4 2 1 356 682–1 357 123 2 Wang et al., 2017 2017 transcription factor 14 A. thaliana L AtCYSa Arabidopsis HORVU1Hr1G067870.2 56 Cysteine proteinase inhibitor 1 479 563 716–479 564 368 Zhang et al., 2008 2008 A. thaliana L AtCYSb Arabidopsis HORVU3Hr1G038190.1 66 Cysteine proteinase inhibitor 12 3 219 953 557–219 956 556 Zhang et al., 2008 2008 A. thaliana L AtNHX1 Cotton HORVU2Hr1G021020.4 69 Sodium hydrogen exchanger 2 2 59 025 629–59 030 226 Cheng C et al., 2018 2018 A. thaliana L AtPP2-B11 Arabidopsis HORVU6Hr1G090000.1 42 F-box protein PP2-B1 6 571 135 647–571 137 859 Jia et al., 2015 2015 A. thaliana L AnnAt8 Arabidopsis HORVU6Hr1G074440.1 50 Annexin 7 6 514 097 241–514 103 959 Yadav et al., 2016 2016 A. thaliana L AtDIF1 Arabidopsis HORVU5Hr1G079500.1 42 Sister chromatid cohesion 1 protein 4 1 557 145 143–557 147 352 Gao et al., 2017 2017 A. thaliana L NF-YA1-9 Arabidopsis HORVU5Hr1G007890.11 66 Nuclear transcription factor Y subunit A-10 5 16 694 492–16 699 091 Mu et al., 2013 2013 Maize ( Zea mays ) ZmCBL4 Arabidopsis HORVU1Hr1G080820.6 72 Calcineurin B-like protein 8 1 526 318 770–526 320 885 Wang MY et al., 2007 2007 2 Maize ( Z. mays ) 2 ZmMKK4 2 Arabidopsis 2 HORVU0Hr1G038850.2 2 88 Protein kinase superfamily 2 0 2 247 582 088–247 583 184 2 Kong et al., 2011 2011 protein 2 Maize ( Z. mays ) 2 ZmMPK5 2 Tobacco 2 HORVU7Hr1G023760.3 2 89 Mitogen-activated protein 2 7 2 37 300 015–37 306 217 2 Zhang et al., 2014 2014 kinase 3 2 Rice ( Oryza sativa ) 2 OSISAP1 2 Tobacco 2 HORVU5Hr1G072920.1 2 70 Zinc finger A20 and AN1 2 5 2 536 933 399–536 936 238 Mukhopadhyay domain-containing stress-associated protein 1 et al., 2004 2 Rice ( O. sativa ) 2 OsDREB2A 2 Soybean 2 HORVU6Hr1G050520.2 2 78 Ethylene-responsive 2 6 2 306 973 236–306 973 949 2 Zhang et al., 2013 2013 transcription factor 4 2 Rice ( O. sativa ) 2 OsiSAP8 2 Tobacco/rice 2 HORVU2Hr1G053670.4 2 43 Zinc finger A20 and AN1 2 2 2 328 713 964–328 714 708 2 Kanneganti and Gupta, 2008 2008 domain-containing stress-associated protein 9 Rice ( O. sativa ) OsMYB48-1 Rice HORVU1Hr1G008810.3 82 MYB domain protein 59 1 19 369 578–19 370 912 Xiong et al., 2014 2014 2 Rice ( O. sativa ) 2 OsSAP11 2 Arabidopsis 2 HORVU7Hr1G050270.3 2 66 Zinc finger A20 and AN1 2 7 2 180 473 211–180 476 075 2 Giri et al., 2011 2011 domain-containing stress-associated protein 11 Rice ( O. sativa OsRLCK253 Arabidopsis HORVU6Hr1G061280.1 69 Protein kinase superfamily protein 6 410 507 581–410 509 354 Giri et al., 2011 2011 2 Rice ( O. sativa ) 2 OsGSTU4 2 Arabidopsis 2 HORVU6Hr1G026810.3 2 71 Glutathione S-transferase 2 6 2 103 574 244–103 575 543 2 Sharma et al., 2014 2014 family protein Rice ( O. sativa ) OsDREB1D Arabidopsis HORVU5Hr1G080420.1 71 C-repeat-binding factor 4 5 560 569 797–560 571 193 Zhang et al., 2009 2009 Rice ( O. sativa ) OsNAC9 Rice HORVU7Hr1G060310.1 75 NAC domain protein 7 276 430 981–276 436 993 Redillas et al., 2012 2012 2 Rice ( O. sativa ) 2 OsZFP179 2 Rice 2 HORVU5Hr1G055970.1 2 85 RING/U-box superfamily 2 5 2 438 292 337–438 301 123 2 Sun et al., 2010 2010 protein 2 Rice ( O. sativa ) 2 OsOPT10 Arabidopsis/ 2 HORVU6Hr1G067430.2 2 30 2 Oligopeptide transporter 4 2 6 2 467 362 064–467 373 338 2 Jung et al., 2010 2010 rice Rice ( O. sativa ) OsMYB3R-2 Arabidopsis HORVU3Hr1G086270.3 71 MYB domain protein 3R-5 3 616 465 321–616 471 572 Dai et al., 2007 2007 Soybean ( Glycine max ) GmbZIP44 Arabidopsis HORVU5Hr1G023000.1 43 Basic-leucine zipper transcription factor family protein 5 119 817 528–119 818 004 Liao et al., 2008 2008 Soybean ( G. max ) GmbZIP62 Arabidopsis HORVU6Hr1G031330.2 49 Basic-leucine zipper transcription factor family protein 6 132 098 841–132 101 167 Liao et al., 2008 2008 Soybean ( G. max ) GmbZIP78 Arabidopsis HORVU2Hr1G055230.4 61 Basic-leucine zipper 8 2 342 114 231–342 120 751 Liao et al., 2008 2008 2 Soybean ( G. max ) 2 GmDREB2 Arabidopsis/ 2 HORVU4Hr1G015350.1 2 66 2 Ethylene-responsive transcription factor 2 2 4 2 59 331 360–59 332 535 2 Chen M et al., 2007 2007 tobacco Soybean ( G. max ) GmDREB1 Wheat HORVU7Hr1G026940.1 67 Ethylene-responsive transcription factor 5 7 47 357 790–47 359 063 Jiang et al., 2014 2014 2 Soybean ( G. max ) 2 GmNARK 2 Arabidopsis 2 HORVU5Hr1G098840.2 2 54 Leucine-rich receptor-like 2 5 2 608 904 210–608 907 733 2 Cheng CH et al., 2018 2018 protein kinase family protein 2 Soybean ( G. max ) 2 GmFDL19 2 Soybean 2 HORVU2Hr1G110500.1 2 76 ABSCISIC ACID- 2 2 2 720 057 018–720 058 296 2 Li et al., 2017 2017 INSENSITIVE 5-like protein 5 Wheat ( Triticum aestivum ) TaNAC29 Arabidopsis HORVU2Hr1G017470.1 93 NAC domain protein 2 42 672 748–42 675 686 Huang et al., 2015 2015 Wheat ( T. aestivum ) TaSC Arabidopsis HORVU5Hr1G067740.1 99 Transmembrane protein 50A 5 514 305 842–514 309 764 Huang et al., 2012 2012 Wheat ( T. aestivum ) TaNAC2D Arabidopsis HORVU5Hr1G111590.2 95 NAC domain protein 5 636 772 274–636 774 317 Huang and Wang, 2016 2016 Wheat ( T. aestivum ) TaARGOS Arabidopsis HORVU4Hr1G043960.1 88 Eukaryotic aspartyl protease family protein 4 351 442 597–351 444 197 Zhao et al., 2017 2017 Wheat ( T. aestivum ) TaCRT1 Tobacco HORVU3Hr1G089830.2 98 Calreticulin 3 3 630 039 636–630 043 684 Xiang et al., 2015 2015 2 Wheat ( T. aestivum ) 2 TaSRG Arabidopsis/ 2 HORVU2Hr1G072420.11 2 97 2 Family of unknown function (DUF662) 2 2 2 519 528 221–519 529 717 2 He et al., 2011 2011 rice Wheat ( T. aestivum ) TaSTRG Tobacco HORVU4Hr1G063430.1 90 Salt-tolerance-related protein 4 531 361 349–531 362 720 Kavas et al., 2016 2016 Wheat ( T. aestivum ) DHN-5 Arabidopsis HORVU5Hr1G103460.2 79 Dehydrin Rab15 5 616 115 076–616 116 086 Brini et al., 2007 2007 Wheat ( T. aestivum ) TaAQP8 Tobacco HORVU2Hr1G096360.13 91 Aquaporin-like superfamily protein 2 674 156 225–674 158 128 Hu et al., 2012 2012 Wheat ( T. aestivum ) TaWRKY10 Tobacco HORVU2Hr1G109330.1 87 WRKY family transcription factor 2 716 404 110–716 405 772 Wang et al., 2013 2013 2 Wheat ( T. aestivum ) 2 TaDi19A 2 Arabidopsis 2 HORVU3Hr1G061690.1 2 97 Protein DEHYDRATION- 2 3 2 469 768 135–469 771 916 2 Li et al., 2010 2010 INDUCED 19 homolog 3 Wheat ( T. aestivum ) TaWD40D Arabidopsis HORVU0Hr1G016450.1 99 Transducin/WD40 repeat-like superfamily protein 0 88 366 914–88 373 289 Kong et al., 2015 2015 Wheat ( T. aestivum ) TaAIDFa Arabidopsis HORVU5Hr1G105980.4 72 Histone-lysine N -methyltransferase NSD3 5 623 061 366–623 067 662 Xu et al., 2008a 2008a Wheat ( T. aestivum ) TaCIPK29 Tobacco HORVU2Hr1G018340.3 92 Protein kinase family protein 2 46 669 169–46 672 779 Deng et al., 2013 2013 2 Wheat ( T. aestivum ) 2 TaERF3 2 Wheat 2 HORVU2Hr1G098330.1 2 85 Ethylene-responsive 2 2 2 682 511 166–682 511 937 2 Rong et al., 2014 2014 transcription factor 1 Wheat ( T. aestivum ) TaPUB1 Tobacco HORVU4Hr1G083960.3 95 Pre-mRNA-processing factor 19 3 627 004 064–627 010 259 Zhang et al., 2017 2017 Wheat ( T. aestivum ) TaWRKY44 Tobacco HORVU4Hr1G048400.12 92 WRKY DNA-binding protein 3 4 390 705 028–390 708 928 Wang et al., 2015 2015 Wheat ( T. aestivum ) TaVB Arabidopsis HORVU4Hr1G033760.1 97 Sodium hydrogen exchanger 2 4 238 472 323–238 482 634 Wang et al., 2011 2011 Wheat ( T. aestivum ) TaSRHP Arabidopsis HORVU7Hr1G037410.4 90 Protein of unknown function 7 89 779 039–89 780 525 Hou et al., 2013 2013 Wheat ( T. aestivum ) TaNHXS1 Tobacco HORVU2Hr1G021020.4 70 Sodium hydrogen exchanger 2 2 59 025 629–59 030 226 Gouiaa et al., 2012 2012 2 Wheat ( T. aestivum ) 2 TaVP1 2 Tobacco 2 HORVU7Hr1G031480.1 2 97 K + -insensitive pyrophosphate- 2 7 2 63 936 492–63 936 858 2 Gouiaa et al., 2012 2012 energized proton pump Wheat ( T. aestivum ) HORVU7Hr1G114250.2 88 Pyrophosphate-energized vacuolar membrane proton pump 7 639 161 697–639 164 555 Gouiaa et al., 2012 2012 Wheat ( T. aestivum ) TaPLDα Arabidopsis HORVU1Hr1G048970.4 100 Phospholipase D P2 1 363 556 495–363 563 036 Wang et al., 2014 2014 Wheat ( T. aestivum ) TaOPR1 Arabidopsis HORVU1Hr1G001850.3 82 12-Oxophytodienoate reductase 2 1 4 131 150–4 132 543 Dong et al., 2013 2013 Wheat ( T. aestivum ) TaNF-YA10-1 Arabidopsis HORVU6Hr1G081080.12 89 Nuclear transcription factor Y subunit A-5 6 544 207 949–544 211 747 Ma et al., 2015 2015 Wheat ( T. aestivum ) TaPI4KIIγ Arabidopsis HORVU2Hr1G118320.7 94 Phosphatidylinositol 3- and 4-kinase family protein 2 742 201 795–742 204 374 Liu et al., 2013 2013 Barley salinity tolerance characterized transcriptional factors and genes during germination 2 A highly positive correlation has been reported between salinity stress and polyethylene glycol treatments, indicating that salt stress in germinating seed is mostly osmotic (Mano et al., 1996 1996 ). Therefore, osmoprotection is the likely early response in barley geminating seeds (Walia et al., 2006 2006 ). 4.2.1 6PGDH and Glc/RibDH Salinity tolerant lines at germination in a mapping population containing 94 DH lines of DOM/REC expressed a higher level of 6-phosphogluconate dehydrogenase (6PGDH) and glucose/ribitol dehydrogenase (Glc/RibDH) in mature seeds (Witzel et al., 2010 2010 ). Overexpression of the two enzymes in yeast enhanced the growth of transformed cells in saline media (Witzel et al., 2010 2010 ). Cytosolic 6PGDH is an enzyme participating in the pentose phosphate pathway, which provides reduced nicotinamide adenine dinucleotide phosphate (NADPH) as an electron donor in the reductive biosynthetic process, and is important for the ascorbate–glutathione synthesis phase in the plant antioxidant protection system (Corpas et al., 1998 1998 ). This protein concentration is increased under salinity stress in olive (Valderrama et al., 2006 2006 ) and rice (Huang et al., 2003 2003 ; Hou et al., 2007 2007 ). Transcripts and protein Glc/RibDH are short alcohol dehydrogenases (Jornvall et al., 1984 1984 ) found in developing barley embryos, whose level of transcription reduces with germination (Alexander et al., 1994 1994 ), and which catalyse the oxidation of D -glucose to synthesize sugars for osmoprotective functions (Witzel et al., 2010 2010 ). 4.2.2 Dehydrins Dehydrins (DHNs), a subfamily of LEA proteins from Hordeum vulgare ( aba2 ), enhanced seed germination in transgenic lines of Arabidopsis under salinity stress, relative to the wild type (Calestani et al., 2015 2015 ). Similar protein-coding genes have been identified in wheat ( Dhn5 ) and maize ( Rab17 ) with comparable results when overexpressed in transgenic Arabidopsis plants (Figueras et al., 2004 2004 ; Brini et al., 2011 2011 ). DHNs are thought to be involved in protecting the embryo through seed desiccation and rehydration (Skriver and Mundy, 1990 1990 ; Blackman et al., 1991 1991 ; Tunnacliffe and Wise, 2007 2007 ) by increasing their contents during the last phase of seed development, and in dormant embryos. DHN content decreases when imbibition and germination begin as seeds lose their capacity to withstand desiccation (Blackman et al., 1991 1991 ; Han et al., 1997 1997 ). DHNs also facilitate water uptake during seed germination on media with low osmotic potential (Hara, 2010 2010 ), and may act as a hydration buffer inside cells in the presence of sugars (Walters et al., 1997 1997 ; Hara, 2010 2010 ). Moreover, they are likely to play a role in cellular detoxification because they contain lipids and metal-binding capacity that can prevent lipid peroxidation (Cheng et al., 2002 2002 ; Krüger et al., 2002 2002 ; Alsheikh et al., 2003 2003 ; Koag et al., 2003 2003 , 2009 2009 ). 4.2.3 CBLs Rice transgenic lines with CBL protein 8 ( HsCBL8 ) transferred from wild barley homolog to HvCBL8 of cultivated barley improved seed germination, reduced Na + uptake, adjusted K + concentration in tissues, provided in vivo water protection of the plasma membrane, and accumulated more proline under salt stress (Guo et al., 2016 2016 ). The build-up of compatible osmolytes, like proline, is linked to stress tolerance in plants (Ahmed et al., 2013b 2013b ; Mekawy et al., 2015 2015 ). Phylogenetic analysis of HsCBL8 showed that it encodes proteins of the CBL group modified with only N-myristoylation or S-acylation (Batistič et al., 2012 2012 ). Such proteins are involved in relationships with the transmembrane (TM) helix (Kleist et al., 2014 2014 ) including HvCBL8 . Reports about other CBLs from different plant species reflected similar trends to that of HsCBL8 , such as transgenic Arabidopsis having 35S-AtCBL5 (Cheong et al., 2010 2010 ) and poplar harbouring 35S-PeCBL10 (Li DD et al., 2013 2013 ). OsCBL2 is likely to be involved in GA-signalling that facilitates the vacuolation of aleurone cells (Hwang et al., 2005 2005 ), and AtCBL1 is involved in upregulation of GA (Li ZY et al., 2013 2013 ) and downregulation of ABA (Pandey et al., 2008 2008 ) during seed germination. 4.2.4 SERKs Three orthologs of somatic embryogenesis receptor-like kinase (SERK) genes ( HvSERK1 / 2 / 3 ) isolated from barley were induced in microspore-derived embryogenic callus under salt stress (Li et al., 2016 2016 ), indicating their protective role for developing embryos during salinity stress. SERKs are a subfamily of the leucine-rich repeat receptor-like kinase II group (LRR-RLKII) with proline-rich SPP motifs between the LRRs and the TM domain (Hecht et al., 2001 2001 ). These genes are present during somatic embryogenesis in plants before declining in later stages (Schmidt et al., 1997 1997 ; Somleva et al., 2000 2000 ; Nolan et al., 2003 2003 ; Singla et al., 2008 2008 ; Li, 2010 2010 ). They have been characterized in many plants, including maize (Baudino et al., 2001 2001 ), wheat (Singla et al., 2008 2008 ), soybean (Yang et al., 2011 2011 ), rice (Singla et al., 2009 2009 ), cotton (Pandey and Chaudhary, 2014 2014 ), and Arabidopsis (Hecht et al., 2001 2001 ). In rice ( Oryza sativa L.), BRs reverse the inhibitory effect of salinity during germination (Anuradha and Rao, 2001 2001 ), and in Arabidopsis are reportedly signalled by SERK1 , SERK3 , and SERK4 (Albrecht et al., 2008 2008 ), while ABA stimulates OsSERK1 during stress (Hu et al., 2005 2005 ). 4.2.5 DREBs A gene that encodes DREB proteins in H . vulgare ( HvDREB1 ) is induced by exogenous ABA to enhance germination and early root growth in Arabidopsis plants under salinity stress (Xue et al., 2004 2004 ). TF HvDREB1 is a member of the AP2 group of the DREB subfamily that is vital for regulating responses to various stresses (Agarwal et al., 2006 2006 ; Xu et al., 2008b 2008b ) and reportedly improves salt, drought, and cold responses in transgenic plants (Oh et al., 2007 2007 ). Overexpressing rice OsDREB1A in Arabidopsis enhanced tolerance to drought and freezing stresses (Dubouzet et al., 2003 2003 ), and barley’s HvCBF4 in rice transgenes increased drought, salt, and cold stress tolerance (Oh et al., 2007 2007 ). DREB proteins isolated from several plants including rice, maize, soybean, and wheat are involved in several signal transduction pathways during abiotic stress (Dubouzet et al., 2003 2003 ; Agarwal et al., 2006 2006 ). Of particular interest are those belonging to the A-2 group that respond to dehydration and salinity stress (Liu et al., 1998 1998 ; Dubouzet et al., 2003 2003 ) and regulate ABA-independent gene expression in target plants under stress (Chinnusamy et al., 2006 2006 ; Nakashima and Yamaguchi-Shinozaki, 2006 2006 ). It is possible that HvDREB1 may take part in both ABA-independent and -dependent pathways concurrently (Xue et al., 2004 2004 ). 4.2.6 ERFs Barley ERF-type TF HvRAF improved seed germination and root growth under salinity stress but was not induced by ABA treatment in transgenic Arabidopsis plants (Jung et al., 2007 2007 ). TF HvRAF is a member of the AP2 group in the ERF family (Sakuma et al., 2002 2002 ; Gutterson and Reuber, 2004 2004 ), which is involved in regulating both biotic and abiotic stress-responsive genes in plants (Lee et al., 2004 2004 ; Yi et al., 2004 2004 ). However, the response of Arabidopsis transgenic lines with HvRAF was specific to salinity stress, where it acted as a regulator for ABA-independent signalling in root growth and seed germination (Jung et al., 2007 2007 ). Similar ABA regulation responses to salinity have been documented in Arabidopsis for DREB2A and DREB2B (Chinnusamy et al., 2005 2005 ). A tolerance response in terms of root growth and seed germination was observed when CaERFLP1 and JERF1 from pepper and tomato, respectively, were overexpressed in transgenic tobacco plants in response to salt stress (Lee et al., 2004 2004 ; Zhang et al., 2004 2004 ). 4.2.7 Aquaporin genes Overexpression of a barley aquaporin gene HvPIP2;5 in yeast enhanced salt and osmotic stress tolerance, and transgenic Arabidopsis with the gene showed better seed germination and root growth than the wild type under salinity stress (Alavilli et al., 2016 2016 ). Aquaporins form part of the major intrinsic proteins (MIPs) found in living organisms that enable the transportation of water and small nonpolar molecules across living membranes (Zardoya et al., 2002 2002 ; Maurel et al., 2015 2015 ). In plants, all but the GlpF-like intrinsic proteins show water-specific channel movement. Hence, the collective name for MIPs in plants is aquaporins (Maurel et al., 2008 2008 ), even though they can transport additional small molecules such as CO 2 and ammonia inside cells (Uehlein et al., 2003 2003 ; Jahn et al., 2004 2004 ). There are five groups of aquaporins in plant genomes, reflective of their diverse physiological roles. Of importance are the plasma membrane intrinsic proteins (PIPs) that are further subdivided into PIP1 and PIP2, each with several isoforms (Javot et al., 2003 2003 ; Postaire et al., 2010 2010 ). Overexpression of PIP genes from various plants ( O . sativa , Nicotiana tabacum , Vicia faba , Arabidopsis , and Triticum aestivum ) enhanced dehydration stress tolerance in their respective transgenic lines (Alavilli et al., 2016 2016 ). Diversity of barley salinity tolerance genes at germination 2 In this review, we have compared studies to determine whether any of the eight genes (Table 3 3 ) that have been reported and functionally characterized for salinity tolerance in barley at germination are unique or similar to their homologs from wheat and rice. All the sequences producing a significant match, based on length and total relationship hits, were downloaded and recorded. The following total significant homolog hits from barley, wheat, and rice were recorded: dehydrins (17), dehydrogenase/reductase SDR family member 4 (20), 6PGDH, (29), ERFs (31), CBL protein (72), DREB protein (164), SERKs (215), and aquaporin gene (227). The protein sequences of identified functional barley genes retrieved from BARLEX (https://apex.ipk-gatersleben.de/apex/f?p=284:10) and blasted on barley (https://webblast.ipk-gatersleben.de/barley_ibsc/viroblast.php), wheat (https://urgi.versailles.inra.fr/blast_iwgsc/?dbgroup=wheat_iwgsc_refseq_v1_chromosomes & program=blastn), and rice (https:// www.plantgdb.org/OsGDB www.plantgdb.org/OsGDB ) genome explorers Reported functional barley gene 2 Gene ID in barley 3 Gene name in barley 6-Phosphogluconate dehydrogenase 2 HORVU7Hr1G006160.4 3 6-Phosphogluconate dehydrogenase, decarboxylating 1 Glucose/ribitol dehydrogenase 2 HORVU1Hr1G018140.5 3 Dehydrogenase/reductase SDR family member 4 Dehydrin 2 HORVU7Hr1G099800.5 3 Dihydroneopterin aldolase Calcineurin B-like protein 8 2 HORVU1Hr1G064470.4 3 Calcineurin B-like protein 1 Somatic embryogenesis receptor-like kinase 2 HORVU7Hr1G068990.2 3 Receptor-like protein kinase 4 Dehydration-responsive element binding protein 2 HORVU3Hr1G017950.4 3 Chromodomain-helicase-DNA-binding protein 5 Ethylene response factor 2 HORVU4Hr1G077310.1 3 Ethylene-responsive transcription factor 1 Aquaporin gene 2 HORVU2Hr1G089940.1 3 Aquaporin-like superfamily protein 6 6 Reported functional barley gene Reported gene ID 2 Chromosome Location Reference 6 6-Phosphogluconate dehydrogenase 6PGDH 2 7 8 000 958–8 002 650 Witzel et al., 2010 2010 Glucose/ribitol dehydrogenase Glc / RibDH 2 1 65 592 292–65 593 858 Witzel et al., 2010 2010 Dehydrin aba2 2 7 602 554 874–602 555 971 Calestani et al., 2015 2015 Calcineurin B-like protein 8 HvCBL8 2 1 461 521 906–461 524 442 Guo et al., 2016 2016 Somatic embryogenesis receptor-like kinase HvSERK1 / 2 / 3 2 7 366 099 333–366 114 129 Li et al., 2016 2016 Dehydration-responsive element binding protein HvDREB1 2 3 46 482 481–46 494 788 Xue et al., 2004 2004 Ethylene response factor HvRAF 2 4 603 804 858–603 809 470 Jung et al., 2007 2007 Aquaporin gene HvPIP2;5 2 2 640 763 978–640 768 942 Alavilli et al., 2016 2016 Three genes families—DREB protein, SERKs and aquaporin gene—were considered for further analysis based on their high numbers of hits. The proteins from the three genes were blasted on the Phytozome (https://phytozome.jgi.doe.gov/pz/portal. html) to download matched homologs ( > 30%) in 40 different plant species. Mega software (https:// www www . megasoftware.net) was used to align the 40 species’ sequences, and a phylogenetic tree was constructed to estimate the evolutionary distances between the genes using MEGA-X software (https:// www.megasoftware www.megasoftware . net) (Kumar et al., 2018 2018 ). Gene alignments showed three distinct regions across the sequences of the gene families. The start and end sections of the sequences were more divergent than the middle segments. The phylogenetic tree of the DREB proteins divided the genes into two major groups that were further divided into two subgroups (Fig. 2a 2a ). The groups were distinguished by the presence or absence of genes from wheat, barley, and rice. Among the four sub-groups, barley genes appeared three times in two categories while genes from the three cereals were missing in two sub-groups (Fig. 2a 2a ). The phylogenetic tree shows that DREB proteins are no more diverse in barley than in wheat or rice. The SERK phylogenetic tree (Fig. 2b 2b ) was similar to that of the DREB proteins, but with more hits. However, the four subgroups contained genes from the three cereals with five hits for barley and wheat, and three hits for rice. The aquaporin gene phylogenetic tree differed from the other two trees in which the genes were first divided into three major groups, two small and one major, containing representative genes from the three cereals (Fig. 3 3 ). (a) Dehydration-responsive element binding proteins. (b) Somatic embryogenesis receptor-like kinases. The unrooted phylogenetic trees of 37 (a) and 92 (b) domains comprising four (a) and five (b) domains, respectively, from barley were constructed using MEGA-X The unrooted phylogenetic tree of 74 domains comprising five domains from barley was constructed using MEGA-X Conclusions and future prospects 1 Among the most destructive abiotic stresses, salinity causes massive yield losses in crops in arid, semi-arid, coastal regions, and humid and sub-humid landscapes. Thus, more effort is needed to increase crop yields in these areas to produce enough food for the increasing global population. Growing salt-adapted cultivars requires knowledge of the donating characters at different growth stages. It involves the use of many disciplines to identify and functionally characterize the genes contributing to tolerance, and then to transfer them to commercially acceptable cultivars. Barley is one of the hardiest crops that can grow in saline environments, but its germination is severely affected by salinity stress. Development of cultivars that can acclimatise to salinity at this stage is essential in regions like Western Australia that experience hot and dry summers and increasing salt levels in the topsoil before sowing in autumn. The identification and characterization of salinity tolerance genes, enzymes, and compounds during germination in barley have been ongoing, and some transgenic “salt-tolerant” plants have been developed. However, the seeds of these genotypes have had little success in commercial production because they are not equipped with holistic genes or the mechanisms required for successful germination and growth under saline field conditions. This review summarized the agronomic/morphological, physiological, and biochemical traits related to salinity stress. The best trait or combination of traits needs to be identified which can be used to accurately screen for salinity stress tolerance at germination to identify and characterize novel genes. Homolog salinity tolerance genes in barley during germination have been reported, but they need to be validated in barley and other transgenic plants that carry them. Functional characterization by blending genetic, agronomic, biochemical, and physiological indicators can facilitate proof of identity of the genes, leading to the development of barley cultivars with improved salt tolerance at germination and better performance in the field. References WAE Abido , A Allem , L Zsombic , 等 . Effect of gibberellic acid on germination of six wheat cultivars under salinity stress levels . Asian J Biol Sci , 2019 . 12 ( 1 ): 51 - 60 . DOI: 10.3923/ajbs.2019.51.60 http://doi.org/10.3923/ajbs.2019.51.60 . Effect of gibberellic acid on germination of six wheat cultivars under salinity stress levels IP Abrol , JSP Yadav , FI Massoud . Salt-Affected Soils and Their Management , 1988 . FAO Soils Bulletin 39, Food and Agriculture Organization of the United Nations, Rome , . Salt-Affected Soils and Their Management PK Agarwal , B Jha . Transcription factors in plants and ABA dependent and independent abiotic stress signalling . Biol Plant , 2010 . 54 ( 2 ): 201 - 212 . DOI: 10.1007/s10535-010-0038-7 http://doi.org/10.1007/s10535-010-0038-7 . Transcription factors in plants and ABA dependent and independent abiotic stress signalling PK Agarwal , P Agarwal , MK Reddy , 等 . Role of DREB transcription factors in abiotic and biotic stress tolerance in plants . Plant Cell Rep , 2006 . 25 ( 12 ): 1263 - 1274 . 16858552 DOI: 10.1007/s00299-006-0204-8 http://doi.org/10.1007/s00299-006-0204-8 . Role of DREB transcription factors in abiotic and biotic stress tolerance in plants PK Agarwal , PS Shukla , K Gupta , 等 . Bioengineering for salinity tolerance in plants: state of the art . Mol Biotechnol , 2013 . 54 ( 1 ): 102 - 123 . 22539206 DOI: 10.1007/s12033-012-9538-3 http://doi.org/10.1007/s12033-012-9538-3 . Bioengineering for salinity tolerance in plants: state of the art IM Ahmed , FB Cao , M Zhang , 等 . Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys . PLoS ONE , 2013 . 8 ( 10 ): e77869 24205003 DOI: 10.1371/journal.pone.0077869 http://doi.org/10.1371/journal.pone.0077869 . Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys IM Ahmed , HX Dai , WT Zheng , 等 . Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley . Plant Physiol Biochem , 2013 . 63 49 - 60 . 23232247 DOI: 10.1016/j.plaphy.2012.11.004 http://doi.org/10.1016/j.plaphy.2012.11.004 . Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley H Alavilli , JP Awasthi , GR Rout , 等 . Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants . Front Plant Sci, 7:1566 , 2016 . DOI: 10.3389/fpls.2016.01566 http://doi.org/10.3389/fpls.2016.01566 . Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants C Albrecht , E Russinova , B Kemmerling , 等 . Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways . Plant Physiol , 2008 . 148 ( 1 ): 611 - 619 . 18667726 DOI: 10.1104/pp.108.123216 http://doi.org/10.1104/pp.108.123216 . Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways R Alexander , JM Alamillo , F Salamini , 等 . A novel embryo-specific barley cDNA clone encodes a protein with homologies to bacterial glucose and ribitol dehydrogenase . Planta , 1994 . 192 ( 4 ): 519 - 525 . 7764620 DOI: 10.1007/BF00203590 http://doi.org/10.1007/BF00203590 . A novel embryo-specific barley cDNA clone encodes a protein with homologies to bacterial glucose and ribitol dehydrogenase AN Alhasnawi . Role of proline in plant stress tolerance: a mini review . Res Crops , 2019 . 20 ( 1 ): 223 - 229 . . Role of proline in plant stress tolerance: a mini review E Ali , N Hussain , IH Shamsi , 等 . Role of jasmonic acid in improving tolerance of rapeseed ( Brassica napus L.) to Cd toxicity . J Zhejiang Univ-Sci B (Biomed & Biotechnol) , 2018 . 19 ( 2 ): 130 - 146 . DOI: 10.1631/jzus.B1700191 http://doi.org/10.1631/jzus.B1700191 . Role of jasmonic acid in improving tolerance of rapeseed (Brassica napus L.) to Cd toxicity GN al-Karaki . Germination, sodium, and potassium concentrations of barley seeds as influenced by salinity . J Plant Nutr , 2001 . 24 ( 3 ): 511 - 522 . DOI: 10.1081/PLN-100104976 http://doi.org/10.1081/PLN-100104976 . Germination, sodium, and potassium concentrations of barley seeds as influenced by salinity MK Alsheikh , BJ Heyen , SK Randall . Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation . J Biol Chem , 2003 . 278 ( 42 ): 40882 - 40889 . 12917402 DOI: 10.1074/jbc.M307151200 http://doi.org/10.1074/jbc.M307151200 . Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation A al-Yassin , R Khademian . Allelic variation of salinity tolerance genes in barley ecotypes (natural populations) using EcoTILLING: a review article . Am Eur J Agric Environ Sci , 2015 . 15 ( 4 ): 563 - 572 . DOI: 10.5829/idosi.aejaes.2015.15.4.12579 http://doi.org/10.5829/idosi.aejaes.2015.15.4.12579 . Allelic variation of salinity tolerance genes in barley ecotypes (natural populations) using EcoTILLING: a review article TT Angessa , XQ Zhang , GF Zhou , 等 . Early growth stages salinity stress tolerance in CM72×Gairdner doubled haploid barley population . PLoS ONE , 2017 . 12 ( 6 ): e0179715 28640858 DOI: 10.1371/journal.pone.0179715 http://doi.org/10.1371/journal.pone.0179715 . Early growth stages salinity stress tolerance in CM72×Gairdner doubled haploid barley population HP Anosheh , H Sadeghi , Y Emam . Chemical priming with urea and KNO 3 enhances maize hybrids ( Zea mays L.) seed viability under abiotic stress . J Crop Sci Biotechnol , 2011 . 14 ( 4 ): 289 - 295 . DOI: 10.1007/s12892-011-0039-x http://doi.org/10.1007/s12892-011-0039-x . Chemical priming with urea and KNO3 enhances maize hybrids (Zea mays L.) seed viability under abiotic stress S Anuradha , SSR Rao . Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice ( Oryza sativa L.) . Plant Growth Regul , 2001 . 33 ( 2 ): 151 - 153 . DOI: 10.1023/A:1017590108484 http://doi.org/10.1023/A:1017590108484 . Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.) A Arora . Ethylene receptors and molecular mechanism of ethylene sensitivity in plants . Curr Sci , 2005 . 89 ( 8 ): 1348 - 1361 . . Ethylene receptors and molecular mechanism of ethylene sensitivity in plants M Ashraf . Biotechnological approach of improving plant salt tolerance using antioxidants as markers . Biotechnol Adv , 2009 . 27 ( 1 ): 84 - 93 . 18950697 DOI: 10.1016/j.biotechadv.2008.09.003 http://doi.org/10.1016/j.biotechadv.2008.09.003 . Biotechnological approach of improving plant salt tolerance using antioxidants as markers M Ashraf , PJC Harris . Potential biochemical indicators of salinity tolerance in plants . Plant Sci , 2004 . 166 ( 1 ): 3 - 16 . DOI: 10.1016/j.plantsci.2003.10.024 http://doi.org/10.1016/j.plantsci.2003.10.024 . Potential biochemical indicators of salinity tolerance in plants M Ashraf , PJC Harris . Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches , 2005 . Haworth Press, New York, USA , . Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches M Ashraf , NA Akram , RN Arteca , 等 . The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance . Crit Rev Plant Sci , 2010 . 29 ( 3 ): 162 - 190 . DOI: 10.1080/07352689.2010.483580 http://doi.org/10.1080/07352689.2010.483580 . The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance DVM Assaha , A Ueda , H Saneoka , 等 . The role of Na + and K + transporters in salt stress adaptation in glycophytes . Front Physiol, 8:509 , 2017 . DOI: 10.3389/fphys.2017.00509 http://doi.org/10.3389/fphys.2017.00509 . The role of Na+ and K+ transporters in salt stress adaptation in glycophytes A Bajguz , S Hayat . Effects of brassinosteroids on the plant responses to environmental stresses . Plant Physiol Biochem , 2009 . 47 ( 1 ): 1 - 8 . 19010688 DOI: 10.1016/j.plaphy.2008.10.002 http://doi.org/10.1016/j.plaphy.2008.10.002 . Effects of brassinosteroids on the plant responses to environmental stresses D Bartels , D Nelson . Approaches to improve stress tolerance using molecular genetics . Plant Cell Environ , 1994 . 17 ( 5 ): 659 - 667 . DOI: 10.1111/j.1365-3040.1994.tb00157.x http://doi.org/10.1111/j.1365-3040.1994.tb00157.x . Approaches to improve stress tolerance using molecular genetics CC Baskin , JM Baskin . Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination , 2001 . Academic Press, San Diego, USA , DOI: 10.1016/B978-0-12-080260-9.X5000-3 http://doi.org/10.1016/B978-0-12-080260-9.X5000-3 . Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination O Batistič , M Rehers , A Akerman , 等 . S-acylation-dependent association of the calcium sensor CBL2 with the vacuolar membrane is essential for proper abscisic acid responses . Cell Res , 2012 . 22 ( 7 ): 1155 - 1168 . 22547024 DOI: 10.1038/cr.2012.71 http://doi.org/10.1038/cr.2012.71 . S-acylation-dependent association of the calcium sensor CBL2 with the vacuolar membrane is essential for proper abscisic acid responses S Baudino , S Hansen , R Brettschneider , 等 . Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family . Planta , 2001 . 213 ( 1 ): 1 - 10 . 11523644 DOI: 10.1007/s004250000471 http://doi.org/10.1007/s004250000471 . Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family C Belin , L Lopez-Molina . Arabidopsis seed germination responses to osmotic stress involve the chromatin modifier PICKLE . Plant Signal Behav , 2008 . 3 ( 7 ): 478 - 479 . 19704491 DOI: 10.4161/psb.3.7.5679 http://doi.org/10.4161/psb.3.7.5679 . Arabidopsis seed germination responses to osmotic stress involve the chromatin modifier PICKLE DA Benson , M Cavanaugh , K Clark , 等 . GenBank . Nucleic Acids Res , 2013 . 41 ( D1 ): D36 - D42 . 23193287 DOI: 10.1093/nar/gks1195 http://doi.org/10.1093/nar/gks1195 . GenBank L Bentsink , M Koornneef . Seed dormancy and germination . Arabidopsis Book, 6:e0119 , 2008 . DOI: 10.1199/tab.0119 http://doi.org/10.1199/tab.0119 . Seed dormancy and germination L Bernstein . Osmotic adjustment of plants to saline media. II. Dynamic phase . Am J Bot , 1963 . 50 ( 4 ): 360 - 370 . DOI: 10.1002/j.1537-2197.1963.tb07204.x http://doi.org/10.1002/j.1537-2197.1963.tb07204.x . Osmotic adjustment of plants to saline media. II. Dynamic phase JD Bewley . Seed germination and dormancy . Plant Cell , 1997 . 9 ( 7 ): 1055 - 1066 . 12237375 DOI: 10.1105/tpc.9.7.1055 http://doi.org/10.1105/tpc.9.7.1055 . Seed germination and dormancy JD Bewley , KJ Bradford , HWM Hilhorst , 等 . Seeds: Physiology of Development, Germination and Dormancy, 3rd Ed , 2013 . Springer, New York, USA , DOI: 10.1007/978-1-4614-4693-4 http://doi.org/10.1007/978-1-4614-4693-4 . Seeds: Physiology of Development, Germination and Dormancy, 3rd Ed SA Blackman , SH Wettlaufer , RL Obendorf , 等 . Maturation proteins associated with desiccation tolerance in soybean . Plant Physiol , 1991 . 96 ( 3 ): 868 - 874 . 16668267 DOI: 10.1104/pp.96.3.868 http://doi.org/10.1104/pp.96.3.868 . Maturation proteins associated with desiccation tolerance in soybean RD Bliss , KA Platt-Aloia , WW Thomson . Osmotic sensitivity in relation to salt sensitivity in germinating barley seeds . Plant Cell Environ , 1986 . 9 ( 9 ): 721 - 725 . DOI: 10.1111/j.1365-3040.1986.tb02104.x http://doi.org/10.1111/j.1365-3040.1986.tb02104.x . Osmotic sensitivity in relation to salt sensitivity in germinating barley seeds A Bordi . The influence of salt stress on seed germination, growth and yield of canola cultivars . Not Bot Hort Agrobot Cluj , 2010 . 38 ( 1 ): 128 - 133 . . The influence of salt stress on seed germination, growth and yield of canola cultivars F Brini , M Hanin , V Lumbreras , 等 . Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana . Plant Cell Rep , 2007 . 26 ( 11 ): 2017 - 2026 . 17641860 DOI: 10.1007/s00299-007-0412-x http://doi.org/10.1007/s00299-007-0412-x . Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana F Brini , A Yamamoto , L Jlaiel , 等 . Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis . Plant Cell Physiol , 2011 . 52 ( 4 ): 676 - 688 . 21421569 DOI: 10.1093/pcp/pcr030 http://doi.org/10.1093/pcp/pcr030 . Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis C Calestani , MS Moses , E Maestri , 等 . Constitutive expression of the barley dehydrin gene aba2 enhances Arabidopsis germination in response to salt stress . Int J Plant Biol , 2015 . 6 ( 1 ): 5826 DOI: 10.4081/pb.2015.5826 http://doi.org/10.4081/pb.2015.5826 . Constitutive expression of the barley dehydrin gene aba2 enhances Arabidopsis germination in response to salt stress DA Capiati , SM Pais , MT Téllez-Iñón . Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling . J Exp Bot , 2006 . 57 ( 10 ): 2391 - 2400 . 16766597 DOI: 10.1093/jxb/erj212 http://doi.org/10.1093/jxb/erj212 . Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling M Chen , QY Wang , XG Cheng , 等 . GmDREB2 , a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants . Biochem Biophys Res Commun , 2007 . 353 ( 2 ): 299 - 305 . 17178106 DOI: 10.1016/j.bbrc.2006.12.027 http://doi.org/10.1016/j.bbrc.2006.12.027 . GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants ZH Chen , TA Cuin , MX Zhou , 等 . Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance . J Exp Bot , 2007 . 58 ( 15-16 ): 4245 - 4255 . 18182428 DOI: 10.1093/jxb/erm284 http://doi.org/10.1093/jxb/erm284 . Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance C Cheng , Y Zhang , XG Chen , 等 . Co-expression of AtNHX1 and TsVP improves the salt tolerance of transgenic cotton and increases seed cotton yield in a saline field . Mol Breeding , 2018 . 38 ( 2 ): 19 DOI: 10.1007/s11032-018-0774-5 http://doi.org/10.1007/s11032-018-0774-5 . Co-expression of AtNHX1 and TsVP improves the salt tolerance of transgenic cotton and increases seed cotton yield in a saline field CH Cheng , CM Li , DD Wang , 等 . The soybean GmNARK affects ABA and salt responses in transgenic Arabidopsis thaliana . Front Plant Sci, 9:514 , 2018 . DOI: 10.3389/fpls.2018.00514 http://doi.org/10.3389/fpls.2018.00514 . The soybean GmNARK affects ABA and salt responses in transgenic Arabidopsis thaliana ZQ Cheng , J Targolli , XQ Huang , 等 . Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice ( Oryza sativa L.) . Mol Breed , 2002 . 10 ( 1-2 ): 71 - 82 . DOI: 10.1023/A:1020329401191 http://doi.org/10.1023/A:1020329401191 . Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.) YH Cheong , SJ Sung , BG Kim , 等 . Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis . Mol Cells , 2010 . 29 ( 2 ): 159 - 165 . 20077023 DOI: 10.1007/s10059-010-0025-z http://doi.org/10.1007/s10059-010-0025-z . Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis V Chinnusamy , A Jagendorf , JK Zhu . Understanding and improving salt tolerance in plants . Crop Sci , 2005 . 45 ( 2 ): 437 - 448 . DOI: 10.2135/cropsci2005.0437 http://doi.org/10.2135/cropsci2005.0437 . Understanding and improving salt tolerance in plants V Chinnusamy , JH Zhu , JK Zhu . Gene regulation during cold acclimation in plants . Physiol Plant , 2006 . 126 ( 1 ): 52 - 61 . DOI: 10.1111/j.1399-3054.2006.00596.x http://doi.org/10.1111/j.1399-3054.2006.00596.x . Gene regulation during cold acclimation in plants SDS Chiwocha , AJ Cutler , SR Abrams , 等 . The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination . Plant J , 2005 . 42 ( 1 ): 35 - 48 . 15773852 DOI: 10.1111/j.1365-313X.2005.02359.x http://doi.org/10.1111/j.1365-313X.2005.02359.x . The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination C Colmsee , S Beier , A Himmelbach , 等 . BARLEX the barley draft genome explorer . Mol Plant , 2015 . 8 ( 6 ): 964 - 966 . 25804976 DOI: 10.1016/j.molp.2015.03.009 http://doi.org/10.1016/j.molp.2015.03.009 . BARLEX the barley draft genome explorer FJ Corpas , JB Barroso , LM Sandalio , 等 . A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes . Biochem J , 1998 . 330 ( 2 ): 777 - 784 . 9480890 DOI: 10.1042/bj3300777 http://doi.org/10.1042/bj3300777 . A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes XY Dai , YY Xu , QB Ma , 等 . Overexpression of an R1R2R3 MYB gene, OsMYB3R-2 , increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis . Plant Physiol , 2007 . 143 ( 4 ): 1739 - 1751 . 17293435 DOI: 10.1104/pp.106.094532 http://doi.org/10.1104/pp.106.094532 . Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis A Debez , IDB Slimen , S Bousselmi , 等 . Comparative analysis of salt impact on sea barley from semi-arid habitats in Tunisia and cultivated barley with special emphasis on reserve mobilization and stress recovery aptitude . Plant Biosyst, published online , 2019 . DOI: 10.1080/11263504.2019.1651777 http://doi.org/10.1080/11263504.2019.1651777 . Comparative analysis of salt impact on sea barley from semi-arid habitats in Tunisia and cultivated barley with special emphasis on reserve mobilization and stress recovery aptitude XM Deng , W Hu , SY Wei , 等 . TaCIPK29 , a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco . PLoS ONE , 2013 . 8 ( 7 ): e69881 23922838 DOI: 10.1371/journal.pone.0069881 http://doi.org/10.1371/journal.pone.0069881 . TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco M Diaz-Mendoza , I Diaz , M Martinez . Insights on the proteases involved in barley and wheat grain germination . Int J Mol Sci , 2019 . 20 ( 9 ): 2087 DOI: 10.3390/ijms20092087 http://doi.org/10.3390/ijms20092087 . Insights on the proteases involved in barley and wheat grain germination CJ Diédhiou , OV Popova , KJ Dietz , 等 . The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice . BMC Plant Biol, 8:49 , 2008 . DOI: 10.1186/1471-2229-8-49 http://doi.org/10.1186/1471-2229-8-49 . The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice GL Dodd , LA Donovan . Water potential and ionic effects on germination and seedling growth of two cold desert shrubs . Am J Bot , 1999 . 86 ( 8 ): 1146 - 1153 . 10449394 DOI: 10.2307/2656978 http://doi.org/10.2307/2656978 . Water potential and ionic effects on germination and seedling growth of two cold desert shrubs W Dong , MC Wang , F Xu , 等 . Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging . Plant Physiol , 2013 . 161 ( 3 ): 1217 - 1228 . 23321418 DOI: 10.1104/pp.112.211854 http://doi.org/10.1104/pp.112.211854 . Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging JG Dubouzet , Y Sakuma , Y Ito , 等 . OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression . Plant J , 2003 . 33 ( 4 ): 751 - 763 . 12609047 DOI: 10.1046/j.1365-313X.2003.01661.x http://doi.org/10.1046/j.1365-313X.2003.01661.x . OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression AAA el-Mashad , HI Mohamed . Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants ( Vigna sinensis ) . Protoplasma , 2012 . 249 ( 3 ): 625 - 635 . 21732069 DOI: 10.1007/s00709-011-0300-7 http://doi.org/10.1007/s00709-011-0300-7 . Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis) Y Emam , E Hosseini , N Rafiei , 等 . Response of early growth and sodium and potassium concentration in ten barley ( Hordeum vulgare L.) cultivars under salt stress conditions . Crop Physiol J , 2013 . 19 5 - 15 . . Response of early growth and sodium and potassium concentration in ten barley (Hordeum vulgare L.) cultivars under salt stress conditions NV Fedoroff . Cross-talk in abscisic acid signaling . Sci STKE , 2002 . 10 ( 140 ): re10 DOI: 10.1126/stke.2002.140.re10 http://doi.org/10.1126/stke.2002.140.re10 . Cross-talk in abscisic acid signaling M Figueras , J Pujal , A Saleh , 等 . Maize Rabl7 overexpression in Arabidopsis plants promotes osmotic stress tolerance . Ann Appl Biol , 2004 . 144 ( 3 ): 251 - 257 . DOI: 10.1111/j.1744-7348.2004.tb00341.x http://doi.org/10.1111/j.1744-7348.2004.tb00341.x . Maize Rabl7 overexpression in Arabidopsis plants promotes osmotic stress tolerance WE Finch-Savage , G Leubner-Metzger . Seed dormancy and the control of germination . New Phytol , 2006 . 171 ( 3 ): 501 - 523 . 16866955 DOI: 10.1111/j.1469-8137.2006.01787.x http://doi.org/10.1111/j.1469-8137.2006.01787.x . Seed dormancy and the control of germination TJ Flowers , MA Hajibagheri . Salinity tolerance in Hordeum vulgare : ion concentrations in root cells of cultivars differing in salt tolerance . Plant Soil , 2001 . 231 ( 1 ): 1 - 9 . DOI: 10.1023/A:1010372213938 http://doi.org/10.1023/A:1010372213938 . Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance LB Fu , QF Shen , LH Kuang , 等 . Metabolite profiling and gene expression of Na/K transporter analyses reveal mechanisms of the difference in salt tolerance between barley and rice . Plant Physiol Biochem , 2018 . 130 248 - 257 . 30021179 DOI: 10.1016/j.plaphy.2018.07.013 http://doi.org/10.1016/j.plaphy.2018.07.013 . Metabolite profiling and gene expression of Na/K transporter analyses reveal mechanisms of the difference in salt tolerance between barley and rice S Gao , JB Song , Y Wang , 等 . An F-box E3 ubiquitin ligase-coding gene AtDIF1 is involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner . Environ Exp Bot , 2017 . 138 21 - 35 . DOI: 10.1016/j.envexpbot.2017.02.013 http://doi.org/10.1016/j.envexpbot.2017.02.013 . An F-box E3 ubiquitin ligase-coding gene AtDIF1 is involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner F Ghassemi , AJ Jakeman , HA Nix . Salinisation of Land and Water Resources: Human Causes, Extent, Management and Case Studies , 1995 . CAB International, Wallingford, UK , . Salinisation of Land and Water Resources: Human Causes, Extent, Management and Case Studies J Giri , S Vij , PK Dansana , 等 . Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants . New Phytol , 2011 . 191 ( 3 ): 721 - 732 . 21534973 DOI: 10.1111/j.1469-8137.2011.03740.x http://doi.org/10.1111/j.1469-8137.2011.03740.x . Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants EP Glenn , JJ Brown , E Blumwald . Salt tolerance and crop potential of halophytes . Crit Rev Plant Sci , 1999 . 18 ( 2 ): 227 - 255 . DOI: 10.1080/07352689991309207 http://doi.org/10.1080/07352689991309207 . Salt tolerance and crop potential of halophytes S Gouiaa , H Khoudi , EO Leidi , 等 . Expression of wheat Na + /H + antiporter TNHXS1 and H + -pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance . Plant Mol Biol , 2012 . 79 ( 1-2 ): 137 - 155 . 22415161 DOI: 10.1007/s11103-012-9901-6 http://doi.org/10.1007/s11103-012-9901-6 . Expression of wheat Na+/H+ antiporter TNHXS1 and H+-pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance K Graeber , A Linkies , K Müller , 等 . Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes . Plant Mol Biol , 2010 . 73 ( 1-2 ): 67 - 87 . 20013031 DOI: 10.1007/s11103-009-9583-x http://doi.org/10.1007/s11103-009-9583-x . Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes H Greenway , R Munns . Mechanisms of salt tolerance in nonhalophytes . Ann Rev Plant Physiol , 1980 . 31 149 - 190 . DOI: 10.1146/annurev.pp.31.060180.001053 http://doi.org/10.1146/annurev.pp.31.060180.001053 . Mechanisms of salt tolerance in nonhalophytes E Grotewold . Transcription factors for predictive plant metabolic engineering: are we there yet? . Curr Opin Biotechnol , 2008 . 19 ( 2 ): 138 - 144 . 18374558 DOI: 10.1016/j.copbio.2008.02.002 http://doi.org/10.1016/j.copbio.2008.02.002 . Transcription factors for predictive plant metabolic engineering: are we there yet? WL Guo , TL Chen , N Hussain , 等 . Characterization of salinity tolerance of transgenic rice lines harboring HsCBL8 of wild barley ( Hordeum spontanum ) line from Qinghai-Tibet Plateau . Front Plant Sci, 7:1678 , 2016 . DOI: 10.3389/fpls.2016.01678 http://doi.org/10.3389/fpls.2016.01678 . Characterization of salinity tolerance of transgenic rice lines harboring HsCBL8 of wild barley (Hordeum spontanum) line from Qinghai-Tibet Plateau B Gupta , BR Huang . Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization . Int J Genomics, 2014:701596 , 2014 . DOI: 10.1155/2014/701596 http://doi.org/10.1155/2014/701596 . Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization F Gürel , ZN Öztürk , C Uçarlı , 等 . Barley genes as tools to confer abiotic stress tolerance in crops . Front Plant Sci, 7:1137 , 2016 . DOI: 10.3389/fpls.2016.01137 http://doi.org/10.3389/fpls.2016.01137 . Barley genes as tools to confer abiotic stress tolerance in crops N Gutterson , TL Reuber . Regulation of disease resistance pathways by AP2/ERF transcription factors . Curr Opin Plant Biol , 2004 . 7 ( 4 ): 465 - 471 . 15231271 DOI: 10.1016/j.pbi.2004.04.007 http://doi.org/10.1016/j.pbi.2004.04.007 . Regulation of disease resistance pathways by AP2/ERF transcription factors CR Hampson , GM Simpson . Effects of temperature, salt, and osmotic potential on early growth of wheat ( Triticum aestivum ). I. Germination . Can J Bot , 1990 . 68 ( 3 ): 524 - 528 . DOI: 10.1139/b90-072 http://doi.org/10.1139/b90-072 . Effects of temperature, salt, and osmotic potential on early growth of wheat (Triticum aestivum). I. Germination B Han , DW Hughes , GA Galau , 等 . Changes in late-embryogenesis-abundant (LEA) messenger RNAs and dehydrins during maturation and premature drying of Ricinus communis L. seeds . Planta , 1997 . 201 ( 1 ): 27 - 35 . 9004548 DOI: 10.1007/BF01258677 http://doi.org/10.1007/BF01258677 . Changes in late-embryogenesis-abundant (LEA) messenger RNAs and dehydrins during maturation and premature drying of Ricinus communis L. seeds Y Han , SY Yin , L Huang . Towards plant salinity tolerance-implications from ion transporters and biochemical regulation . Plant Growth Regul , 2015 . 76 ( 1 ): 13 - 23 . DOI: 10.1007/s10725-014-9997-6 http://doi.org/10.1007/s10725-014-9997-6 . Towards plant salinity tolerance-implications from ion transporters and biochemical regulation Y Han , SY Yin , L Huang , 等 . A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis . Plant Cell Physiol , 2018 . 59 ( 10 ): 1976 - 1989 . 29917153 DOI: 10.1093/pcp/pcy116 http://doi.org/10.1093/pcp/pcy116 . A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis M Hanin , C Ebel , M Ngom , 等 . New insights on plant salt tolerance mechanisms and their potential use for breeding . Front Plant Sci, 7:1787 , 2016 . DOI: 10.3389/fpls.2016.01787 http://doi.org/10.3389/fpls.2016.01787 . New insights on plant salt tolerance mechanisms and their potential use for breeding M Hara . The multifunctionality of dehydrins: an overview . Plant Signal Behav , 2010 . 5 ( 5 ): 503 - 508 . 20139737 DOI: 10.4161/psb.11085 http://doi.org/10.4161/psb.11085 . The multifunctionality of dehydrins: an overview JR Harlan . The Living Fields: Our Agricultural Heritage , 1995 . Cambridge University Press, Cambridge, UK , . The Living Fields: Our Agricultural Heritage PM Hasegawa , RA Bressan , JK Zhu , 等 . Plant cellular and molecular responses to high salinity . Annu Rev Plant Physiol Plant Mol Biol , 2000 . 51 463 - 499 . 15012199 DOI: 10.1146/annurev.arplant.51.1.463 http://doi.org/10.1146/annurev.arplant.51.1.463 . Plant cellular and molecular responses to high salinity AL Hauvermale , T Ariizumi , CM Steber . Gibberellin signaling: a theme and variations on DELLA repression . Plant Physiol , 2012 . 160 ( 1 ): 83 - 92 . 22843665 DOI: 10.1104/pp.112.200956 http://doi.org/10.1104/pp.112.200956 . Gibberellin signaling: a theme and variations on DELLA repression KM Hazzouri , B Khraiwesh , KMA Amiri , 等 . Mapping of HKT1;5 gene in barley using GWAS approach and its implication in salt tolerance mechanism . Front Plant Sci, 9:156 , 2018 . DOI: 10.3389/fpls.2018.00156 http://doi.org/10.3389/fpls.2018.00156 . Mapping of HKT1;5 gene in barley using GWAS approach and its implication in salt tolerance mechanism XL He , XN Hou , YZ Shen , 等 . TaSRG , a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis . FEBS Lett , 2011 . 585 ( 8 ): 1231 - 1237 . 21457711 DOI: 10.1016/j.febslet.2011.03.055 http://doi.org/10.1016/j.febslet.2011.03.055 . TaSRG, a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis V Hecht , JP Vielle-Calzada , MV Hartog , 等 . The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture . Plant Physiol , 2001 . 127 ( 3 ): 803 - 816 . 11706164 DOI: 10.1104/pp.010324 http://doi.org/10.1104/pp.010324 . The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture M Hentrich , C Böttcher , P Düchting , 等 . The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression . Plant J , 2013 . 74 ( 4 ): 626 - 637 . 23425284 DOI: 10.1111/tpj.12152 http://doi.org/10.1111/tpj.12152 . The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression JA Hernández , MA Ferrer , A Jiménez , 等 . Antioxidant systems and O 2 · − /H 2 O 2 production in the apoplast of pea leaves. its relation with salt-induced necrotic lesions in minor veins . Plant Physiol , 2001 . 127 ( 3 ): 817 - 831 . 11706165 DOI: 10.1104/pp.010188 http://doi.org/10.1104/pp.010188 . Antioxidant systems and O2·−/H2O2 production in the apoplast of pea leaves. its relation with salt-induced necrotic lesions in minor veins FY Hou , J Huang , SL Yu , 等 . The 6-phosphogluconate dehydrogenase genes are responsive to abiotic stresses in rice . J Integr Plant Biol , 2007 . 49 ( 5 ): 655 - 663 . DOI: 10.1111/j.1744-7909.2007.00460.x http://doi.org/10.1111/j.1744-7909.2007.00460.x . The 6-phosphogluconate dehydrogenase genes are responsive to abiotic stresses in rice XN Hou , YZ Liang , XL He , 等 . A novel ABA-responsive TaSRHP gene from wheat contributes to enhanced resistance to salt stress in Arabidopsis thaliana . Plant Mol Biol Rep , 2013 . 31 ( 4 ): 791 - 801 . DOI: 10.1007/s11105-012-0549-9 http://doi.org/10.1007/s11105-012-0549-9 . A novel ABA-responsive TaSRHP gene from wheat contributes to enhanced resistance to salt stress in Arabidopsis thaliana GL Hoyle , KJ Steadman , RB Good , 等 . Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits . Front Plant Sci, 6:731 , 2015 . DOI: 10.3389/fpls.2015.00731 http://doi.org/10.3389/fpls.2015.00731 . Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits H Hu , L Xiong , Y Yang . Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection . Planta , 2005 . 222 ( 1 ): 107 - 117 . 15968510 DOI: 10.1007/s00425-005-1534-4 http://doi.org/10.1007/s00425-005-1534-4 . Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection W Hu , QQ Yuan , Y Wang , 等 . Overexpression of a wheat aquaporin gene, TaAQP8 , enhances salt stress tolerance in transgenic tobacco . Plant Cell Physiol , 2012 . 53 ( 12 ): 2127 - 2141 . 23161856 DOI: 10.1093/pcp/pcs154 http://doi.org/10.1093/pcp/pcs154 . Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco J Huang , HS Zhang , JF Wang , 等 . Molecular cloning and characterization of rice 6-phosphogluconate dehydrogenase gene that is up-regulated by salt stress . Mol Biol Rep , 2003 . 30 ( 4 ): 223 - 227 . 14672408 DOI: 10.1023/A:1026392422995 http://doi.org/10.1023/A:1026392422995 . Molecular cloning and characterization of rice 6-phosphogluconate dehydrogenase gene that is up-regulated by salt stress L Huang , LH Kuang , X Li , 等 . Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare . Environ Exp Bot , 2018 . 156 48 - 61 . DOI: 10.1016/j.envexpbot.2018.08.019 http://doi.org/10.1016/j.envexpbot.2018.08.019 . Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare L Huang , LH Kuang , LY Wu , 等 . Comparisons in functions of HKT1;5 transporters between Hordeum marinum and Hordeum vulgare in responses to salt stress . Plant Growth Regul , 2019 . 89 309 - 319 . DOI: 10.1007/s10725-019-00538-7 http://doi.org/10.1007/s10725-019-00538-7 . Comparisons in functions of HKT1;5 transporters between Hordeum marinum and Hordeum vulgare in responses to salt stress QJ Huang , Y Wang . Overexpression of TaNAC2D displays opposite responses to abiotic stresses between seedling and mature stage of transgenic Arabidopsis . Front Plant Sci, 7:1754 , 2016 . DOI: 10.3389/fpls.2016.01754 http://doi.org/10.3389/fpls.2016.01754 . Overexpression of TaNAC2D displays opposite responses to abiotic stresses between seedling and mature stage of transgenic Arabidopsis QJ Huang , Y Wang , B Li , 等 . TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis . BMC Plant Biol, 15:268 , 2015 . DOI: 10.1186/s12870-015-0644-9 http://doi.org/10.1186/s12870-015-0644-9 . TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis X Huang , Y Zhang , B Jiao , 等 . Overexpression of the wheat salt tolerance-related gene TaSC enhances salt tolerance in Arabidopsis . J Exp Bot , 2012 . 63 ( 15 ): 5463 - 5473 . 22821939 DOI: 10.1093/jxb/ers198 http://doi.org/10.1093/jxb/ers198 . Overexpression of the wheat salt tolerance-related gene TaSC enhances salt tolerance in Arabidopsis YS Hwang , PC Bethke , YH Cheong , 等 . A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function . Plant Physiol , 2005 . 138 ( 3 ): 1347 - 1358 . 15980189 DOI: 10.1104/pp.105.062703 http://doi.org/10.1104/pp.105.062703 . A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function SV Isayenkov . Genetic sources for the development of salt tolerance in crops . Plant Growth Regul , 2019 . 89 ( 1 ): 1 - 17 . DOI: 10.1007/s10725-019-00519-w http://doi.org/10.1007/s10725-019-00519-w . Genetic sources for the development of salt tolerance in crops T Ishikawa , S Shabala . Control of xylem Na + loading and transport to the shoot in rice and barley as a determinant of differential salinity stress tolerance . Physiol Plant , 2019 . 165 ( 3 ): 619 - 631 . 29761494 DOI: 10.1111/ppl.12758 http://doi.org/10.1111/ppl.12758 . Control of xylem Na+ loading and transport to the shoot in rice and barley as a determinant of differential salinity stress tolerance TP Jahn , ALB Møller , T Zeuthen , 等 . Aquaporin homologues in plants and mammals transport ammonia . FEBS Lett , 2004 . 574 ( 1-3 ): 31 - 36 . 15358535 DOI: 10.1016/j.febslet.2004.08.004 http://doi.org/10.1016/j.febslet.2004.08.004 . Aquaporin homologues in plants and mammals transport ammonia F Jalili , K Khavazi , E Pazira , 等 . Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola ( Brassica napus L.) growth . J Plant Physiol , 2009 . 166 ( 6 ): 667 - 674 . 18829132 DOI: 10.1016/j.jplph.2008.08.004 http://doi.org/10.1016/j.jplph.2008.08.004 . Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth A Jamil , S Riaz , M Ashraf , 等 . Gene expression profiling of plants under salt stress . Crit Rev Plant Sci , 2011 . 30 ( 5 ): 435 - 458 . DOI: 10.1080/07352689.2011.605739 http://doi.org/10.1080/07352689.2011.605739 . Gene expression profiling of plants under salt stress WD Jaschke , AD Peuke , JS Pate , 等 . Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean ( Ricinus communis L.) under phosphate deficiency and moderate salinity . J Exp Bot , 1997 . 48 ( 9 ): 1737 - 1747 . DOI: 10.1093/jxb/48.9.1737 http://doi.org/10.1093/jxb/48.9.1737 . Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity H Javot , V Lauvergeat , V Santoni , 等 . Role of a single aquaporin isoform in root water uptake . Plant Cell , 2003 . 15 ( 2 ): 509 - 522 . 12566588 DOI: 10.1105/tpc.008888 http://doi.org/10.1105/tpc.008888 . Role of a single aquaporin isoform in root water uptake M Jayakannan , J Bose , O Babourina , 等 . Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K + loss via a GORK channel . J Exp Bot , 2013 . 64 ( 8 ): 2255 - 2268 . 23580750 DOI: 10.1093/jxb/ert085 http://doi.org/10.1093/jxb/ert085 . Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel MJ Jeong , SK Lee , BG Kim , 等 . A rice ( Oryza sativa L.) MAP kinase gene, OsMAPK44 , is involved in response to abiotic stresses . Plant Cell Tissue Organ Cult , 2006 . 85 ( 2 ): 151 - 160 . DOI: 10.1007/s11240-005-9064-0 http://doi.org/10.1007/s11240-005-9064-0 . A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses FJ Jia , CY Wang , JG Huang , 等 . SCF E3 ligase PP2-B11 plays a positive role in response to salt stress in Arabidopsis . J Exp Bot , 2015 . 66 ( 15 ): 4683 - 4697 . 26041321 DOI: 10.1093/jxb/erv245 http://doi.org/10.1093/jxb/erv245 . SCF E3 ligase PP2-B11 plays a positive role in response to salt stress in Arabidopsis QY Jiang , Z Hu , H Zhang , 等 . Overexpression of GmDREB1 improves salt tolerance in transgenic wheat and leaf protein response to high salinity . Crop J , 2014 . 2 ( 2-3 ): 120 - 131 . DOI: 10.1016/j.cj.2014.02.003 http://doi.org/10.1016/j.cj.2014.02.003 . Overexpression of GmDREB1 improves salt tolerance in transgenic wheat and leaf protein response to high salinity H Jornvall , H von Bahr-Lindstrom , KD Jany , 等 . Extended superfamily of short alcoholpolyol-sugar dehydrogenases: structural similarities between glucose and ribitol dehydrogenases . FEBS Lett , 1984 . 165 ( 2 ): 190 - 196 . 6420186 DOI: 10.1016/0014-5793(84)80167-2 http://doi.org/10.1016/0014-5793(84)80167-2 . Extended superfamily of short alcoholpolyol-sugar dehydrogenases: structural similarities between glucose and ribitol dehydrogenases R Joshi , SH Wani , B Singh , 等 . Transcription factors and plants response to drought stress: current understanding and future directions . Front Plant Sci, 7:1029 , 2016 . DOI: 10.3389/fpls.2016.01029 http://doi.org/10.3389/fpls.2016.01029 . Transcription factors and plants response to drought stress: current understanding and future directions J Jung , SY Won , SC Suh , 等 . The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis . Planta , 2007 . 225 ( 3 ): 575 - 588 . 16937017 DOI: 10.1007/s00425-006-0373-2 http://doi.org/10.1007/s00425-006-0373-2 . The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis YJ Jung , IH Lee , KH Han , 等 . Expression analysis and characterization of rice oligopeptide transport gene ( OsOPT10 ) that contributes to salt stress tolerance . J Plant Biotechnol , 2010 . 37 ( 4 ): 483 - 493 . DOI: 10.5010/JPB.2010.37.4.483 http://doi.org/10.5010/JPB.2010.37.4.483 . Expression analysis and characterization of rice oligopeptide transport gene (OsOPT10) that contributes to salt stress tolerance V Kanneganti , AK Gupta . Overexpression of OsiSAP8 , a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice . Plant Mol Biol , 2008 . 66 ( 5 ): 445 - 462 . 18205020 DOI: 10.1007/s11103-007-9284-2 http://doi.org/10.1007/s11103-007-9284-2 . Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice M Kavas , MC Baloğlu , AM Yücel , 等 . Enhanced salt tolerance of transgenic tobacco expressing a wheat salt tolerance gene . Turk J Biol , 2016 . 40 727 - 735 . DOI: 10.3906/biy-1506-36 http://doi.org/10.3906/biy-1506-36 . Enhanced salt tolerance of transgenic tobacco expressing a wheat salt tolerance gene K Kazan , JM Manners . JAZ repressors and the orchestration of phytohormone crosstalk . Trends Plant Sci , 2012 . 17 ( 1 ): 22 - 31 . 22112386 DOI: 10.1016/j.tplants.2011.10.006 http://doi.org/10.1016/j.tplants.2011.10.006 . JAZ repressors and the orchestration of phytohormone crosstalk BC Keskin , AT Sarikaya , B Yüksel , 等 . Abscisic acid regulated gene expression in bread wheat ( Triticum aestivum L.) . Aust J Crop Sci , 2010 . 4 ( 8 ): 617 - 625 . . Abscisic acid regulated gene expression in bread wheat (Triticum aestivum L.) TJ Kleist , AL Spencley , S Luan . Comparative phylogenomics of the CBL-CIPK calcium-decoding network in the moss Physcomitrella , Arabidopsis, and other green lineages . Front Plant Sci, 5:187 , 2014 . DOI: 10.3389/fpls.2014.00187 http://doi.org/10.3389/fpls.2014.00187 . Comparative phylogenomics of the CBL-CIPK calcium-decoding network in the moss Physcomitrella, Arabidopsis, and other green lineages MC Koag , RD Fenton , S Wilkens , 等 . The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity . Plant Physiol , 2003 . 131 ( 1 ): 309 - 316 . 12529538 DOI: 10.1104/pp.011171 http://doi.org/10.1104/pp.011171 . The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity MC Koag , S Wilkens , RD Fenton , 等 . The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes . Plant Physiol , 2009 . 150 ( 3 ): 1503 - 1514 . 19439573 DOI: 10.1104/pp.109.136697 http://doi.org/10.1104/pp.109.136697 . The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes DJ Kong , MJ Li , ZH Dong , 等 . Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses . Plant Cell Rep , 2015 . 34 ( 3 ): 395 - 410 . 25447637 DOI: 10.1007/s00299-014-1717-1 http://doi.org/10.1007/s00299-014-1717-1 . Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses XP Kong , JW Pan , MY Zhang , 等 . ZmMKK4 , a novel group C mitogen-activated protein kinase kinase in maize ( Zea mays ), confers salt and cold tolerance in transgenic Arabidopsis . Plant Cell Environ , 2011 . 34 ( 8 ): 1291 - 1303 . 21477122 DOI: 10.1111/j.1365-3040.2011.02329.x http://doi.org/10.1111/j.1365-3040.2011.02329.x . ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis M Koornneef , L Bentsink , H Hilhorst . Seed dormancy and germination . Curr Opin Plant Biol , 2002 . 5 ( 1 ): 33 - 36 . 11788305 DOI: 10.1016/S1369-5266(01)00219-9 http://doi.org/10.1016/S1369-5266(01)00219-9 . Seed dormancy and germination S Krishnaswamy , S Verma , MH Rahman , 等 . Functional characterization of four APETALA2-family genes ( RAP2 . 6 , RAP2 . 6L , DREB19 and DREB26 ) in Arabidopsis . Plant Mol Biol , 2011 . 75 ( 1-2 ): 107 - 127 . 21069430 DOI: 10.1007/s11103-010-9711-7 http://doi.org/10.1007/s11103-010-9711-7 . Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis C Krüger , O Berkowitz , UW Stephan , 等 . A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L . J Biol Chem , 2002 . 277 ( 28 ): 25062 - 25069 . 11983700 DOI: 10.1074/jbc.M201896200 http://doi.org/10.1074/jbc.M201896200 . A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L LH Kuang , QF Shen , LY Wu , 等 . Identification of microRNAs responding to salt stress in barley by high-throughput sequencing and degradome analysis . Environ Exp Bot , 2019 . 160 59 - 70 . DOI: 10.1016/j.envexpbot.2019.01.006 http://doi.org/10.1016/j.envexpbot.2019.01.006 . Identification of microRNAs responding to salt stress in barley by high-throughput sequencing and degradome analysis S Kumar , G Stecher , M Li , 等 . MEGA X: molecular evolutionary genetics analysis across computing platforms . Mol Biol Evol , 2018 . 35 ( 6 ): 1547 - 1549 . 29722887 DOI: 10.1093/molbev/msy096 http://doi.org/10.1093/molbev/msy096 . MEGA X: molecular evolutionary genetics analysis across computing platforms N Kumari , K Malik , B Rani , 等 . Varma A Giri B . Insights in the physiological, biochemical and molecular basis of salt stress tolerance in plants . Microorganisms in Saline Environments: Strategies and Functions , 2019 . Springer, Cham , 353 - 374 . DOI: 10.1007/978-3-030-18975-4_15 http://doi.org/10.1007/978-3-030-18975-4_15 . Insights in the physiological, biochemical and molecular basis of salt stress tolerance in plants S Lal , V Gulyani , P Khurana . Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry ( Morus indica ) . Transgenic Res , 2008 . 17 ( 4 ): 651 - 663 . 17932781 DOI: 10.1007/s11248-007-9145-4 http://doi.org/10.1007/s11248-007-9145-4 . Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica) A Läuchli , SR Grattan . Hasegawa PM Jenks MA , Jain SM . Plant growth and development under salinity stress . Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops , 2007 . Springer, Dordrecht , 1 - 32 . DOI: 10.1007/978-1-4020-5578-2_1 http://doi.org/10.1007/978-1-4020-5578-2_1 . Plant growth and development under salinity stress AE Lauchli , E Epstein . Tanji KK . Plant responses to saline and sodic conditions . Agricultural Salinity Assessment and Management , 1990 . ASCE, New York , 113 - 137 . . Plant responses to saline and sodic conditions JH Lee , JP Hong , SK Oh , 等 . The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper ( Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants . Plant Mol Biol , 2004 . 55 ( 1 ): 61 - 81 . 15604665 DOI: 10.1007/s11103-004-0417-6 http://doi.org/10.1007/s11103-004-0417-6 . The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants DD Li , XL Xia , WL Yin , 等 . Two poplar calcineurin B-like proteins confer enhanced tolerance to abiotic stresses in transgenic Arabidopsis thaliana . Biol Plant , 2013 . 57 ( 1 ): 70 - 78 . DOI: 10.1007/s10535-012-0251-7 http://doi.org/10.1007/s10535-012-0251-7 . Two poplar calcineurin B-like proteins confer enhanced tolerance to abiotic stresses in transgenic Arabidopsis thaliana J Li . Multi-tasking of somatic embryogenesis receptor-like protein kinases . Curr Opin Plant Biol , 2010 . 13 ( 5 ): 509 - 514 . 20926334 DOI: 10.1016/j.pbi.2010.09.004 http://doi.org/10.1016/j.pbi.2010.09.004 . Multi-tasking of somatic embryogenesis receptor-like protein kinases SO Li , CH Xu , YA Yang , 等 . Functional analysis of TaDi19A , a salt-responsive gene in wheat . Plant Cell Environ , 2010 . 33 ( 1 ): 117 - 129 . 19895399 DOI: 10.1111/j.1365-3040.2009.02063.x http://doi.org/10.1111/j.1365-3040.2009.02063.x . Functional analysis of TaDi19A, a salt-responsive gene in wheat YB Li , CH Liu , GM Guo , 等 . Expression analysis of three SERK-like genes in barley under abiotic and biotic stresses . J Plant Interact , 2016 . 12 ( 1 ): 279 - 285 . DOI: 10.1080/17429145.2017.1339836 http://doi.org/10.1080/17429145.2017.1339836 . Expression analysis of three SERK-like genes in barley under abiotic and biotic stresses YY Li , QZ Chen , HY Nan , 等 . Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean . PLoS ONE , 2017 . 12 ( 6 ): e0179554 28640834 DOI: 10.1371/journal.pone.0179554 http://doi.org/10.1371/journal.pone.0179554 . Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean ZY Li , ZS Xu , Y Chen , 等 . A novel role for Arabidopsis CBL1 in affecting plant responses to glucose and gibberellin during germination and seedling development . PLoS ONE , 2013 . 8 ( 2 ): e56412 23437128 DOI: 10.1371/journal.pone.0056412 http://doi.org/10.1371/journal.pone.0056412 . A novel role for Arabidopsis CBL1 in affecting plant responses to glucose and gibberellin during germination and seedling development WJ Liang , XL Ma , P Wan , 等 . Plant salt-tolerance mechanism: a review . Biochem Biophys Res Commun , 2018 . 495 ( 1 ): 286 - 291 . 29128358 DOI: 10.1016/j.bbrc.2017.11.043 http://doi.org/10.1016/j.bbrc.2017.11.043 . Plant salt-tolerance mechanism: a review Y Liao , HF Zou , HW Wang , 等 . Soybean GmMYB76 , GmMYB92 , and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants . Cell Res , 2008 . 18 ( 10 ): 1047 - 1060 . 18725908 DOI: 10.1038/cr.2008.280 http://doi.org/10.1038/cr.2008.280 . Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants JP Liu , JK Zhu . A calcium sensor homolog required for plant salt tolerance . Science , 1998 . 280 ( 5371 ): 1943 - 1945 . 9632394 DOI: 10.1126/science.280.5371.1943 http://doi.org/10.1126/science.280.5371.1943 . A calcium sensor homolog required for plant salt tolerance JP Liu , M Ishitani , U Halfter , 等 . The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance . Proc Natl Acad Sci USA , 2000 . 97 ( 7 ): 3730 - 3734 . DOI: 10.1073/pnas.97.7.3730 http://doi.org/10.1073/pnas.97.7.3730 . The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance P Liu , ZS Xu , PP Lu , 等 . A wheat PI4K gene whose product possesses threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis . J Exp Bot , 2013 . 64 ( 10 ): 2915 - 2927 . 23682116 DOI: 10.1093/jxb/ert133 http://doi.org/10.1093/jxb/ert133 . A wheat PI4K gene whose product possesses threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis PP Liu , TA Montgomery , N Fahlgren , 等 . Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages . Plant J , 2007 . 52 ( 1 ): 133 - 146 . 17672844 DOI: 10.1111/j.1365-313X.2007.03218.x http://doi.org/10.1111/j.1365-313X.2007.03218.x . Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages Q Liu , M Kasuga , Y Sakuma , 等 . Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis . Plant Cell , 1998 . 10 ( 8 ): 1391 - 1406 . 9707537 DOI: 10.1105/tpc.10.8.1391 http://doi.org/10.1105/tpc.10.8.1391 . Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis RR Liu , L Wang , M Tanveer , 等 . Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity . Front Plant Sci, 9:1515 , 2018 . DOI: 10.3389/fpls.2018.01515 http://doi.org/10.3389/fpls.2018.01515 . Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity SW Liu , ZY Lv , YH Liu , 等 . Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana . Genet Mol Biol , 2018 . 41 ( 3 ): 624 - 637 . 30044467 DOI: 10.1590/1678-4685-gmb-2017-0229 http://doi.org/10.1590/1678-4685-gmb-2017-0229 . Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana L Lopez-Molina , S Mongrand , NH Chua . A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis . Proc Natl Acad Sci USA , 2001 . 98 ( 8 ): 4782 - 4787 . DOI: 10.1073/pnas.081594298 http://doi.org/10.1073/pnas.081594298 . A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis L Lopez-Molina , S Mongrand , DT McLachlin , 等 . ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination . Plant J , 2002 . 32 ( 3 ): 317 - 328 . 12410810 DOI: 10.1046/j.1365-313X.2002.01430.x http://doi.org/10.1046/j.1365-313X.2002.01430.x . ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination ZH Luan , MX Xiao , DW Zhou , 等 . Effects of salinity, temperature, and polyethylene glycol on the seed germination of sunflower ( Helianthus annuus L.) . Sci World J, 2014:170418 , 2014 . DOI: 10.1155/2014/170418 http://doi.org/10.1155/2014/170418 . Effects of salinity, temperature, and polyethylene glycol on the seed germination of sunflower (Helianthus annuus L.) XY Ma , XL Zhu , CL Li , 等 . Overexpression of wheat NF-YA10 gene regulates the salinity stress response in Arabidopsis thaliana . Plant Physiol Biochem , 2015 . 86 34 - 43 . 25461698 DOI: 10.1016/j.plaphy.2014.11.011 http://doi.org/10.1016/j.plaphy.2014.11.011 . Overexpression of wheat NF-YA10 gene regulates the salinity stress response in Arabidopsis thaliana ZG Ma , NV Bykova , AU Igamberdiev . Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds . Crop J , 2017 . 5 ( 6 ): 459 - 477 . DOI: 10.1016/j.cj.2017.08.007 http://doi.org/10.1016/j.cj.2017.08.007 . Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds RMA Machado , RP Serralheiro . Soil salinity: effect on vegetable crop growth. management practices to prevent and mitigate soil salinization . Horticulturae , 2017 . 3 ( 2 ): 30 DOI: 10.3390/horticulturae3020030 http://doi.org/10.3390/horticulturae3020030 . Soil salinity: effect on vegetable crop growth. management practices to prevent and mitigate soil salinization A Majeed , Z Muhammad . Hakeem KR Hasanuzzaman M , et al Nahar K . Salinity: a major agricultural problem–causes, impacts on crop productivity and management strategies . Plant Abiotic Stress Tolerance , 2019 . Springer, Cham , 83 - 99 . DOI: 10.1007/978-3-030-06118-0_3 http://doi.org/10.1007/978-3-030-06118-0_3 . Salinity: a major agricultural problem–causes, impacts on crop productivity and management strategies G Manchanda , N Garg . Salinity and its effects on the functional biology of legumes . Acta Physiol Plant , 2008 . 30 ( 5 ): 595 - 618 . DOI: 10.1007/s11738-008-0173-3 http://doi.org/10.1007/s11738-008-0173-3 . Salinity and its effects on the functional biology of legumes S Mangano , S Silberstein , GE Santa-María . Point mutations in the barley HvHAK1 potassium transporter lead to improved K + -nutrition and enhanced resistance to salt stress . FEBS Lett , 2008 . 582 ( 28 ): 3922 - 3928 . 18977226 DOI: 10.1016/j.febslet.2008.10.036 http://doi.org/10.1016/j.febslet.2008.10.036 . Point mutations in the barley HvHAK1 potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress Y Mano , K Takeda . Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley ( Hordeum vulgare L.) . Euphytica , 1997 . 94 ( 3 ): 263 - 272 . DOI: 10.1023/A:1002968207362 http://doi.org/10.1023/A:1002968207362 . Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.) Y Mano , H Nakazumi , K Takeda . Varietal variation in and effects of some major genes on salt tolerance at the germination stage in barley . Breed Sci , 1996 . 46 227 - 233 . . Varietal variation in and effects of some major genes on salt tolerance at the germination stage in barley MMF Mansour , EF Ali . Evaluation of proline functions in saline conditions . Phytochemistry , 2017 . 140 52 - 68 . 28458142 DOI: 10.1016/j.phytochem.2017.04.016 http://doi.org/10.1016/j.phytochem.2017.04.016 . Evaluation of proline functions in saline conditions Ichimura MAPK Group , Shinozaki K K . Mitogen-activated protein kinase cascades in plants: a new nomenclature . Trends Plant Sci , 2002 . 7 ( 7 ): 301 - 308 . 12119167 DOI: 10.1016/S1360-1385(02)02302-6 http://doi.org/10.1016/S1360-1385(02)02302-6 . Mitogen-activated protein kinase cascades in plants: a new nomenclature KA Marrs . The functions and regulation of glutathione S-transferases in plants . Annu Rev Plant Physiol Plant Mol Biol , 1996 . 47 127 - 158 . 15012285 DOI: 10.1146/annurev.arplant.47.1.127 http://doi.org/10.1146/annurev.arplant.47.1.127 . The functions and regulation of glutathione S-transferases in plants M Mascher , H Gundlach , A Himmelbach , 等 . A chromosome conformation capture ordered sequence of the barley genome . Nature , 2017 . 544 ( 7651 ): 427 - 433 . 28447635 DOI: 10.1038/nature22043 http://doi.org/10.1038/nature22043 . A chromosome conformation capture ordered sequence of the barley genome AJ Matilla . Ethylene in seed formation and germination . Seed Sci Res , 2000 . 10 ( 2 ): 111 - 126 . DOI: 10.1017/S096025850000012X http://doi.org/10.1017/S096025850000012X . Ethylene in seed formation and germination C Maurel , L Verdoucq , DT Luu , 等 . Plant aquaporins: membrane channels with multiple integrated functions . Annu Rev Plant Biol , 2008 . 59 595 - 624 . 18444909 DOI: 10.1146/annurev.arplant.59.032607.092734 http://doi.org/10.1146/annurev.arplant.59.032607.092734 . Plant aquaporins: membrane channels with multiple integrated functions C Maurel , Y Boursiac , DT Luu , 等 . Aquaporins in plants . Physiol Rev , 2015 . 95 ( 4 ): 1321 - 1358 . 26336033 DOI: 10.1152/physrev.00008.2015 http://doi.org/10.1152/physrev.00008.2015 . Aquaporins in plants AMM Mekawy , DVM Assaha , H Yahagi , 等 . Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress . Plant Physiol Biochem , 2015 . 87 17 - 25 . 25532120 DOI: 10.1016/j.plaphy.2014.12.007 http://doi.org/10.1016/j.plaphy.2014.12.007 . Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress A Mian , RJFJ Oomen , S Isayenkov , 等 . Over-expression of an Na+- and K + -permeable HKT transporter in barley improves salt tolerance . Plant J , 2011 . 68 ( 3 ): 468 - 479 . 21749504 DOI: 10.1111/j.1365-313X.2011.04701.x http://doi.org/10.1111/j.1365-313X.2011.04701.x . Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance M Miransari , DL Smith . Plant hormones and seed germination . Environ Exp Bot , 2014 . 99 110 - 121 . DOI: 10.1016/j.envexpbot.2013.11.005 http://doi.org/10.1016/j.envexpbot.2013.11.005 . Plant hormones and seed germination M Miransari , D Smith . Sustainable wheat ( Triticum aestivum L.) production in saline fields: a review . Crit Rev Biotechnol , 2019 . 39 ( 8 ): 999 - 1014 . 31448647 DOI: 10.1080/07388551.2019.1654973 http://doi.org/10.1080/07388551.2019.1654973 . Sustainable wheat (Triticum aestivum L.) production in saline fields: a review S Mishra , AB Jha , RS Dubey . Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings . Protoplasma , 2011 . 248 ( 3 ): 565 - 577 . 20857150 DOI: 10.1007/s00709-010-0210-0 http://doi.org/10.1007/s00709-010-0210-0 . Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings H Moon , B Lee , G Choi , 等 . NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants . Proc Natl Acad Sci USA , 2003 . 100 ( 1 ): 358 - 363 . DOI: 10.1073/pnas.252641899 http://doi.org/10.1073/pnas.252641899 . NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants JY Mu , HL Tan , SL Hong , 等 . Arabidopsis transcription factor genes NF-YA1 , 5 , 6 , and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development . Mol Plant , 2013 . 6 ( 1 ): 188 - 201 . 22933713 DOI: 10.1093/mp/sss061 http://doi.org/10.1093/mp/sss061 . Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development A Mukhopadhyay , S Vij , AK Tyagi . Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco . Proc Natl Acad Sci USA , 2004 . 101 ( 16 ): 6309 - 6314 . DOI: 10.1073/pnas.0401572101 http://doi.org/10.1073/pnas.0401572101 . Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco R Munns , M Tester . Mechanisms of salinity tolerance . Annu Rev Plant Biol , 2008 . 59 651 - 681 . 18444910 DOI: 10.1146/annurev.arplant.59.032607.092911 http://doi.org/10.1146/annurev.arplant.59.032607.092911 . Mechanisms of salinity tolerance R Munns , PA Gardner , ML Tonnet , 等 . Growth and development in NaCl-treated plants. II. Do Na + or Cl − concentrations in dividing or expanding tissues determine growth in barley? . Aust J Plant Physiol , 1988 . 15 ( 4 ): 529 - 540 . DOI: 10.1071/PP9880529 http://doi.org/10.1071/PP9880529 . Growth and development in NaCl-treated plants. II. Do Na+ or Cl− concentrations in dividing or expanding tissues determine growth in barley? R Munns , RA James , B Xu , 等 . Wheat grain yield on saline soils is improved by an ancestral Na + transporter gene . Nat Biotechnol , 2012 . 30 ( 4 ): 360 - 364 . 22407351 DOI: 10.1038/nbt.2120 http://doi.org/10.1038/nbt.2120 . Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene K Nakashima , K Yamaguchi-Shinozaki . Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants . Physiol Plant , 2006 . 126 ( 1 ): 62 - 71 . DOI: 10.1111/j.1399-3054.2005.00592.x http://doi.org/10.1111/j.1399-3054.2005.00592.x . Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants AM Nalousi , S Ahmadiyan , A Hatamzadeh , 等 . Protective role of exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper ( Capsicum annum L.) . Am Eur J Agric Environ Sci , 2012 . 12 ( 8 ): 1085 - 1090 . DOI: 10.5829/idosi.aejaes.2012.12.08.1938 http://doi.org/10.5829/idosi.aejaes.2012.12.08.1938 . Protective role of exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper (Capsicum annum L.) MP Narsing Rao , ZY Dong , M Xiao , 等 . Varma A Giri B . Effect of salt stress on plants and role of microbes in promoting plant growth under salt stress . Microorganisms in Saline Environments: Strategies and Functions , 2019 . Springer, Cham , 423 - 435 . DOI: 10.1007/978-3-030-18975-4_18 http://doi.org/10.1007/978-3-030-18975-4_18 . Effect of salt stress on plants and role of microbes in promoting plant growth under salt stress K Nawaz . Alleviation of the Adverse Effects of Salinity Stress on Maize ( Zea mays L , 2007 . ) by Exogenous Application of Glycine Betaine. PhD Dissemination, Faculty of Sciences, University of Agriculture, Faisalabad, Pakistan , . Alleviation of the Adverse Effects of Salinity Stress on Maize (Zea mays L S Negrão , SM Schmöckel , M Tester . Evaluating physiological responses of plants to salinity stress . Ann Bot , 2017 . 119 ( 1 ): 1 - 11 . 27707746 DOI: 10.1093/aob/mcw191 http://doi.org/10.1093/aob/mcw191 . Evaluating physiological responses of plants to salinity stress TH Nguyen , HTM To , M Lebrun . Jasmonates–the master regulator of rice development, adaptation and defense . Plants , 2019 . 8 ( 9 ): 339 DOI: 10.3390/plants8090339 http://doi.org/10.3390/plants8090339 . Jasmonates–the master regulator of rice development, adaptation and defense KE Nolan , RR Irwanto , RJ Rose . Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures . Plant Physiol , 2003 . 133 ( 1 ): 218 - 230 . 12970488 DOI: 10.1104/pp.103.020917 http://doi.org/10.1104/pp.103.020917 . Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures SJ Oh , CW Kwon , DW Choi , 等 . Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice . Plant Biotechnol J , 2007 . 5 ( 5 ): 646 - 656 . 17614953 DOI: 10.1111/j.1467-7652.2007.00272.x http://doi.org/10.1111/j.1467-7652.2007.00272.x . Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice DK Pandey , B Chaudhary . Oxidative stress responsive SERK1 gene directs the progression of somatic embryogenesis in cotton ( Gossypium hirsutum L. cv. Coker 310) . Am J Plant Sci , 2014 . 5 ( 1 ): 80 - 102 . DOI: 10.4236/ajps.2014.51012 http://doi.org/10.4236/ajps.2014.51012 . Oxidative stress responsive SERK1 gene directs the progression of somatic embryogenesis in cotton (Gossypium hirsutum L. cv. Coker 310) GK Pandey , JJ Grant , YH Cheong , 等 . Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination . Mol Plant , 2008 . 1 ( 2 ): 238 - 248 . 19825536 DOI: 10.1093/mp/ssn003 http://doi.org/10.1093/mp/ssn003 . Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination JM Pardo , MP Reddy , SL Yang , 等 . Stress signaling through Ca 2+ /calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants . Proc Natl Acad Sci USA , 1998 . 95 ( 16 ): 9681 - 9686 . DOI: 10.1073/pnas.95.16.9681 http://doi.org/10.1073/pnas.95.16.9681 . Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants P Parihar , S Singh , R Singh , 等 . Effect of salinity stress on plants and its tolerance strategies: a review . Environ Sci Pollut Res , 2015 . 22 ( 6 ): 4056 - 4075 . DOI: 10.1007/s11356-014-3739-1 http://doi.org/10.1007/s11356-014-3739-1 . Effect of salinity stress on plants and its tolerance strategies: a review Z Peleg , E Blumwald . Hormone balance and abiotic stress tolerance in crop plants . Curr Opin Plant Biol , 2011 . 14 ( 3 ): 290 - 295 . 21377404 DOI: 10.1016/j.pbi.2011.02.001 http://doi.org/10.1016/j.pbi.2011.02.001 . Hormone balance and abiotic stress tolerance in crop plants S Pennazio , P Roggero . Effects of exogenous salicylate on basal and stress-induced ethylene formation in soybean . Biol Plant , 1991 . 33 ( 1 ): 58 - 65 . DOI: 10.1007/BF02873789 http://doi.org/10.1007/BF02873789 . Effects of exogenous salicylate on basal and stress-induced ethylene formation in soybean L Petruzzelli , I Coraggio , G Leubner-Metzger . Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase . Planta , 2000 . 211 ( 1 ): 144 - 149 . 10923715 DOI: 10.1007/s004250000274 http://doi.org/10.1007/s004250000274 . Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase D Pimentel , B Berger , D Filiberto , 等 . Water resources: agricultural and environmental issues . BioScience , 2004 . 54 ( 10 ): 909 - 918 . DOI: 10.1641/0006-3568(2004)054[0909:WRAAEI]2.0.CO;2 http://doi.org/10.1641/0006-3568(2004)054[0909:WRAAEI]2.0.CO;2 . Water resources: agricultural and environmental issues H Pirasteh-Anosheh , G Ranjbar , H Pakniyat , 等 . Ahmad P Azooz MM . Physiological mechanisms of salt stress tolerance in plants: an overview . Plant-Environment Interaction: Responses and Approaches to Mitigate Stress , 2016 . John Wiley & Sons, Ltd., Chichester, UK , 141 - 160 . DOI: 10.1002/9781119081005.ch8 http://doi.org/10.1002/9781119081005.ch8 . Physiological mechanisms of salt stress tolerance in plants: an overview MAS Polash , A Sakil , A Hossain . Plants responses and their physiological and biochemical defense mechanisms against salinity: a review . Trop Plant Res , 2019 . 6 ( 2 ): 250 - 274 . . Plants responses and their physiological and biochemical defense mechanisms against salinity: a review J Popko , R Hänsch , RR Mendel , 等 . The role of abscisic acid and auxin in the response of poplar to abiotic stress . Plant Biol , 2010 . 12 ( 2 ): 242 - 258 . 20398232 DOI: 10.1111/j.1438-8677.2009.00305.x http://doi.org/10.1111/j.1438-8677.2009.00305.x . The role of abscisic acid and auxin in the response of poplar to abiotic stress LP Popova , ZG Stoinova , LT Maslenkova . Involvement of abscisic acid in photosynthetic process in Hordeum vulgare L. during salinity stress . J Plant Growth Regul , 1995 . 14 ( 4 ): 211 - 218 . DOI: 10.1007/BF00204914 http://doi.org/10.1007/BF00204914 . Involvement of abscisic acid in photosynthetic process in Hordeum vulgare L. during salinity stress O Postaire , C Tournaire-Roux , A Grondin , 等 . A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis . Plant Physiol , 2010 . 152 ( 3 ): 1418 - 1430 . 20034965 DOI: 10.1104/pp.109.145326 http://doi.org/10.1104/pp.109.145326 . A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis P Procházka , P Štranc , I Kupka , 等 . Forest seed treatment with brassinosteroids to increase their germination under stress conditions . J For Sci , 2015 . 61 ( 7 ): 291 - 296 . . Forest seed treatment with brassinosteroids to increase their germination under stress conditions L Qiu , DZ Wu , S Ali , 等 . Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley . Theor Appl Genet , 2011 . 122 ( 4 ): 695 - 703 . 20981400 DOI: 10.1007/s00122-010-1479-2 http://doi.org/10.1007/s00122-010-1479-2 . Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley L Rajjou , M Duval , K Gallardo , 等 . Seed germination and vigor . Annu Rev Plant Biol , 2012 . 63 507 - 533 . 22136565 DOI: 10.1146/annurev-arplant-042811-105550 http://doi.org/10.1146/annurev-arplant-042811-105550 . Seed germination and vigor VS Reddy , ASN Reddy . Proteomics of calcium-signaling components in plants . Phytochemistry , 2004 . 65 ( 12 ): 1745 - 1776 . 15276435 DOI: 10.1016/j.phytochem.2004.04.033 http://doi.org/10.1016/j.phytochem.2004.04.033 . Proteomics of calcium-signaling components in plants MCFR Redillas , JS Jeong , YS Kim , 等 . The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions . Plant Biotechnol J , 2012 . 10 ( 7 ): 792 - 805 . 22551450 DOI: 10.1111/j.1467-7652.2012.00697.x http://doi.org/10.1111/j.1467-7652.2012.00697.x . The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions P Rengasamy . Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview . Aust J Exp Agric , 2002 . 42 ( 3 ): 351 - 361 . DOI: 10.1071/EA01111 http://doi.org/10.1071/EA01111 . Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview P Rengasamy . World salinization with emphasis on Australia . J Exp Bot , 2006 . 57 ( 5 ): 1017 - 1023 . 16510516 DOI: 10.1093/jxb/erj108 http://doi.org/10.1093/jxb/erj108 . World salinization with emphasis on Australia JL Riechmann , J Heard , G Martin , 等 . Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes . Science , 2000 . 290 ( 5499 ): 2105 - 2110 . 11118137 DOI: 10.1126/science.290.5499.2105 http://doi.org/10.1126/science.290.5499.2105 . Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes LMR Rinaldi . Germination of seeds of olive ( Olea europaea L.) and ethylene production: effects of harvesting time and thidiazuron treatment . J Hortic Sci Biotechnol , 2000 . 75 ( 6 ): 727 - 732 . DOI: 10.1080/14620316.2000.11511314 http://doi.org/10.1080/14620316.2000.11511314 . Germination of seeds of olive (Olea europaea L.) and ethylene production: effects of harvesting time and thidiazuron treatment J Rivandi , J Miyazaki , M Hrmova , 等 . A SOS3 homologue maps to HvNax4 , a barley locus controlling an environmentally sensitive Na + exclusion trait . J Exp Bot , 2011 . 62 ( 3 ): 1201 - 1216 . 21047983 DOI: 10.1093/jxb/erq346 http://doi.org/10.1093/jxb/erq346 . A SOS3 homologue maps to HvNax4, a barley locus controlling an environmentally sensitive Na+ exclusion trait JT Romo , MR Haferkamp . Effects of osmotic potential, potassium chloride, and sodium chloride on germination of greasewood ( Sarcobatus vermiculatus ) . Great Basin Nat , 1987 . 47 ( 1 ): 110 - 116 . . Effects of osmotic potential, potassium chloride, and sodium chloride on germination of greasewood (Sarcobatus vermiculatus) W Rong , L Qi , AY Wang , 等 . The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat . Plant Biotechnol J , 2014 . 12 ( 4 ): 468 - 479 . 24393105 DOI: 10.1111/pbi.12153 http://doi.org/10.1111/pbi.12153 . The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat AEL Sabagh , A Hossain , S Islam , 等 . Drought and salinity stresses in barley: consequences and mitigation strategies . Aust J Crop Sci , 2019 . 13 ( 6 ): 810 - 820 . . Drought and salinity stresses in barley: consequences and mitigation strategies H Safdar , A Amin , Y Shafiq , 等 . A review: impact of salinity on plant growth . Nat Sci , 2019 . 17 34 - 40 . . A review: impact of salinity on plant growth Y Sakuma , Q Liu , JG Dubouzet , 等 . DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression . Biochem Biophys Res Commun , 2002 . 290 ( 3 ): 998 - 1009 . 11798174 DOI: 10.1006/bbrc.2001.6299 http://doi.org/10.1006/bbrc.2001.6299 . DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression R Sayar , H Bchini , M Mosbahi , 等 . Effects of salt and drought stresses on germination, emergence and seedling growth of durum wheat ( Triticum durum Desf.) . J Agric Res , 2010 . 5 ( 15 ): 2008 - 2016 . DOI: 10.5897/AJAR09.707 http://doi.org/10.5897/AJAR09.707 . Effects of salt and drought stresses on germination, emergence and seedling growth of durum wheat (Triticum durum Desf.) EDL Schmidt , F Guzzo , MAJ Toonen , 等 . A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos . Development , 1997 . 124 ( 10 ): 2049 - 2062 . 9169851 . A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos D Schulte , TJ Close , A Graner , 等 . The international barley sequencing consortium–at the threshold of efficient access to the barley genome . Plant Physiol , 2009 . 149 ( 1 ): 142 - 147 . 19126706 DOI: 10.1104/pp.108.128967 http://doi.org/10.1104/pp.108.128967 . The international barley sequencing consortium–at the threshold of efficient access to the barley genome PJ Seo , AK Lee , FN Xiang , 等 . Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination . Plant Cell Physiol , 2008 . 49 ( 3 ): 334 - 344 . 18203731 DOI: 10.1093/pcp/pcn011 http://doi.org/10.1093/pcp/pcn011 . Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination S Shabala , S Shabala , TA Cuin , 等 . Xylem ionic relations and salinity tolerance in barley . Plant J , 2010 . 61 ( 5 ): 839 - 853 . 20015063 DOI: 10.1111/j.1365-313X.2009.04110.x http://doi.org/10.1111/j.1365-313X.2009.04110.x . Xylem ionic relations and salinity tolerance in barley R Sharma , A Sahoo , R Devendran , 等 . Over-expression of a rice tau class glutathione S-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis . PLoS ONE , 2014 . 9 ( 3 ): e92900 24663444 DOI: 10.1371/journal.pone.0092900 http://doi.org/10.1371/journal.pone.0092900 . Over-expression of a rice tau class glutathione S-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis QF Shen , JH Yu , LB Fu , 等 . Ionomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in Tibetan wild barley . Plant Physiol Biochem , 2018 . 123 319 - 330 . 29289898 DOI: 10.1016/j.plaphy.2017.12.032 http://doi.org/10.1016/j.plaphy.2017.12.032 . Ionomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in Tibetan wild barley HZ Shi , M Ishitani , C Kim , 等 . The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na + /H + antiporter . Proc Natl Acad Sci USA , 2000 . 97 ( 12 ): 6896 - 6901 . DOI: 10.1073/pnas.120170197 http://doi.org/10.1073/pnas.120170197 . The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter K Shinozaki , K Yamaguchi-Shinozaki . Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways . Curr Opin Plant Biol , 2000 . 3 ( 3 ): 217 - 223 . 10837265 DOI: 10.1016/S1369-5266(00)80068-0 http://doi.org/10.1016/S1369-5266(00)80068-0 . Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways K Shinozaki , K Yamaguchi-Shinozaki . Gene networks involved in drought stress response and tolerance . J Exp Bot , 2007 . 58 ( 2 ): 221 - 227 . 17075077 DOI: 10.1093/jxb/erl164 http://doi.org/10.1093/jxb/erl164 . Gene networks involved in drought stress response and tolerance SH Shiu , MC Shih , WH Li . Transcription factor families have much higher expansion rates in plants than in animals . Plant Physiol , 2005 . 139 ( 1 ): 18 - 26 . 16166257 DOI: 10.1104/pp.105.065110 http://doi.org/10.1104/pp.105.065110 . Transcription factor families have much higher expansion rates in plants than in animals P Shrivastava , R Kumar . Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation . Saudi J Biol Sci , 2015 . 22 ( 2 ): 123 - 131 . 25737642 DOI: 10.1016/j.sjbs.2014.12.001 http://doi.org/10.1016/j.sjbs.2014.12.001 . Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation S Shu , SR Guo , LY Yuan . Najafpour M . A review: polyamines and photosynthesis . Advances in Photosynthesis–Fundamental Aspects , 2012 . IntechOpen, Rijeka, Croatia , 439 - 464 . DOI: 10.5772/26875 http://doi.org/10.5772/26875 . A review: polyamines and photosynthesis B Singla , JP Khurana , P Khurana . Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum . Plant Cell Rep , 2008 . 27 ( 5 ): 833 - 843 . 18210118 DOI: 10.1007/s00299-008-0505-1 http://doi.org/10.1007/s00299-008-0505-1 . Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum B Singla , JP Khurana , P Khurana . Structural characterization and expression analysis of the SERK/SERL gene family in rice ( Oryza sativa ) . Int J Plant Genomics, 2009: 539402 , 2009 . DOI: 10.1155/2009/539402 http://doi.org/10.1155/2009/539402 . Structural characterization and expression analysis of the SERK/SERL gene family in rice (Oryza sativa) K Skriver , J Mundy . Gene expression in response to abscisic acid and osmotic stress . Plant Cell , 1990 . 2 ( 6 ): 503 - 512 . 2152172 DOI: 10.1105/tpc.2.6.503 http://doi.org/10.1105/tpc.2.6.503 . Gene expression in response to abscisic acid and osmotic stress MN Somleva , EDL Schmidt , SC de Vries . Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression . Plant Cell Rep , 2000 . 19 ( 7 ): 718 - 726 . 30754811 DOI: 10.1007/s002999900169 http://doi.org/10.1007/s002999900169 . Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression V Subbiah , KJ Reddy . Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis . J Biosci , 2010 . 35 ( 3 ): 451 - 458 . 20826954 DOI: 10.1007/s12038-010-0050-2 http://doi.org/10.1007/s12038-010-0050-2 . Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis SJ Sun , SQ Guo , X Yang , 等 . Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice . J Exp Bot , 2010 . 61 ( 10 ): 2807 - 2818 . 20460361 DOI: 10.1093/jxb/erq120 http://doi.org/10.1093/jxb/erq120 . Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice TP Sun , F Gubler . Molecular mechanism of gibberellin signaling in plants . Annu Rev Plant Biol , 2004 . 55 197 - 223 . 15377219 DOI: 10.1146/annurev.arplant.55.031903.141753 http://doi.org/10.1146/annurev.arplant.55.031903.141753 . Molecular mechanism of gibberellin signaling in plants M Teige , E Scheikl , T Eulgem , 等 . The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis . Mol Cell , 2004 . 15 ( 1 ): 141 - 152 . 15225555 DOI: 10.1016/j.molcel.2004.06.023 http://doi.org/10.1016/j.molcel.2004.06.023 . The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis International The , Genome Barley , Consortium Sequencing , 等 . A physical, genetic and functional sequence assembly of the barley genome . Nature , 2012 . 491 ( 7426 ): 711 - 716 . 23075845 DOI: 10.1038/nature11543 http://doi.org/10.1038/nature11543 . A physical, genetic and functional sequence assembly of the barley genome A Tunnacliffe , MJ Wise . The continuing conundrum of the LEA proteins . Naturwissenschaften , 2007 . 94 ( 10 ): 791 - 812 . 17479232 DOI: 10.1007/s00114-007-0254-y http://doi.org/10.1007/s00114-007-0254-y . The continuing conundrum of the LEA proteins S Turan , K Cornish , S Kumar . Salinity tolerance in plants: breeding and genetic engineering . Aust J Crop Sci , 2012 . 6 ( 9 ): 1337 - 1348 . . Salinity tolerance in plants: breeding and genetic engineering N Uehlein , C Lovisolo , F Siefritz , 等 . The tobacco aquaporin NtAQP1 is a membrane CO 2 pore with physiological functions . Nature , 2003 . 425 ( 6959 ): 734 - 737 . 14520414 DOI: 10.1038/nature02027 http://doi.org/10.1038/nature02027 . The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions R Valderrama , FJ Corpas , A Carreras , 等 . The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants . Plant Cell Environ , 2006 . 29 ( 7 ): 1449 - 1459 . 17080966 DOI: 10.1111/j.1365-3040.2006.01530.x http://doi.org/10.1111/j.1365-3040.2006.01530.x . The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants MN Vázquez , YR Guerrero , WT de la Noval , 等 . Advances on exogenous applications of brassinosteroids and their analogs to enhance plant tolerance to salinity: a review . Aust J Crop Sci , 2019 . 13 ( 1 ): 115 - 121 . . Advances on exogenous applications of brassinosteroids and their analogs to enhance plant tolerance to salinity: a review A Visioni , A al-Abdallat , JA Elenien , 等 . Sehgal D Rajpal VR , et al Kumar A . Genomics and molecular breeding for improving tolerance to abiotic stress in barley ( Hordeum vulgare L.) . Genomics Assisted Breeding of Crops for Abiotic Stress Tolerance, Vol , 2019 . II. Springer, Cham , 49 - 68 . DOI: 10.1007/978-3-319-99573-1_4 http://doi.org/10.1007/978-3-319-99573-1_4 . Genomics and molecular breeding for improving tolerance to abiotic stress in barley (Hordeum vulgare L.) KM Volkmar , Y Hu , H Steppuhn . Physiological responses of plants to salinity: a review . Can J Plant Sci , 1998 . 78 ( 1 ): 19 - 27 . DOI: 10.4141/P97-020 http://doi.org/10.4141/P97-020 . Physiological responses of plants to salinity: a review H Walia , C Wilson , A Wahid , 等 . Expression analysis of barley ( Hordeum vulgare L.) during salinity stress . Funct Integr Genomics , 2006 . 6 ( 2 ): 143 - 156 . 16450154 DOI: 10.1007/s10142-005-0013-0 http://doi.org/10.1007/s10142-005-0013-0 . Expression analysis of barley (Hordeum vulgare L.) during salinity stress C Walters , JL Ried , MK Walker-Simmons . Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties . Seed Sci Res , 1997 . 7 ( 2 ): 125 - 134 . DOI: 10.1017/S0960258500003469 http://doi.org/10.1017/S0960258500003469 . Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties C Wang , PY Deng , LL Chen , 等 . A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco . PLoS ONE , 2013 . 8 ( 6 ): e65120 23762295 DOI: 10.1371/journal.pone.0065120 http://doi.org/10.1371/journal.pone.0065120 . A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco JB Wang , B Ding , YL Guo , 等 . Overexpression of a wheat phospholipase D gene, TaPLDα , enhances tolerance to drought and osmotic stress in Arabidopsis thaliana . Planta , 2014 . 240 ( 1 ): 103 - 115 . 24705986 DOI: 10.1007/s00425-014-2066-6 http://doi.org/10.1007/s00425-014-2066-6 . Overexpression of a wheat phospholipase D gene, TaPLDα, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana L Wang , XL He , YJ Zhao , 等 . Wheat vacuolar H + -ATPase subunit B cloning and its involvement in salt tolerance . Planta , 2011 . 234 ( 1 ): 1 - 7 . 21344312 DOI: 10.1007/s00425-011-1383-2 http://doi.org/10.1007/s00425-011-1383-2 . Wheat vacuolar H+-ATPase subunit B cloning and its involvement in salt tolerance MY Wang , D Gu , TS Liu , 等 . Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance . Plant Mol Biol , 2007 . 65 ( 6 ): 733 - 746 . 17882512 DOI: 10.1007/s11103-007-9238-8 http://doi.org/10.1007/s11103-007-9238-8 . Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance X Wang , GX Shi , QS Xu , 等 . Exogenous polyamines enhance copper tolerance of Nymphoides peltatum . J Plant Physiol , 2007 . 164 ( 8 ): 1062 - 1070 . 16919365 DOI: 10.1016/j.jplph.2006.06.003 http://doi.org/10.1016/j.jplph.2006.06.003 . Exogenous polyamines enhance copper tolerance of Nymphoides peltatum X Wang , C Hou , K Zheng , 等 . Overexpression of ERF96 , a small ethylene response factor gene, enhances salt tolerance in Arabidopsis . Biol Plant , 2017 . 61 ( 4 ): 693 - 701 . DOI: 10.1007/s10535-017-0734-7 http://doi.org/10.1007/s10535-017-0734-7 . Overexpression of ERF96, a small ethylene response factor gene, enhances salt tolerance in Arabidopsis XT Wang , J Zeng , Y Li , 等 . Expression of TaWRKY44 , a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances . Front Plant Sci, 6:615 , 2015 . DOI: 10.3389/fpls.2015.00615 http://doi.org/10.3389/fpls.2015.00615 . Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances K Weitbrecht , K Müller , G Leubner-Metzger . First off the mark: early seed germination . J Exp Bot , 2011 . 62 ( 10 ): 3289 - 3309 . 21430292 DOI: 10.1093/jxb/err030 http://doi.org/10.1093/jxb/err030 . First off the mark: early seed germination JDB Weyers , NW Paterson . Plant hormones and the control of physiological processes . New Phytol , 2001 . 152 ( 3 ): 375 - 407 . DOI: 10.1046/j.0028-646X.2001.00281.x http://doi.org/10.1046/j.0028-646X.2001.00281.x . Plant hormones and the control of physiological processes Widodo , JH Patterson , E Newbigin , 等 . Metabolic responses to salt stress of barley ( Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance . J Exp Bot , 2009 . 60 ( 14 ): 4089 - 4103 . 19666960 DOI: 10.1093/jxb/erp243 http://doi.org/10.1093/jxb/erp243 . Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance K Witzel , A Weidner , GK Surabhi , 等 . Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination . Plant Cell Environ , 2010 . 33 ( 2 ): 211 - 222 . 19906151 DOI: 10.1111/j.1365-3040.2009.02071.x http://doi.org/10.1111/j.1365-3040.2009.02071.x . Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination DZ Wu , L Qiu , LL Xu , 等 . Genetic variation of HVCBF genes and their association with salinity tolerance in Tibetan annual wild barley . PLoS ONE , 2011 . 6 ( 7 ): e22938 21829562 DOI: 10.1371/journal.pone.0022938 http://doi.org/10.1371/journal.pone.0022938 . Genetic variation of HVCBF genes and their association with salinity tolerance in Tibetan annual wild barley HH Wu , L Shabala , MX Zhou , 等 . Root vacuolar Na + sequestration but not exclusion from uptake correlates with barley salt tolerance . Plant J , 2019 . 100 ( 1 ): 55 - 67 . 31148333 DOI: 10.1111/tpj.14424 http://doi.org/10.1111/tpj.14424 . Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance B Wurzinger , A Mair , B Pfister , 等 . Cross-talk of calcium-dependent protein kinase and MAP kinase signaling . Plant Signal Behav , 2011 . 6 ( 1 ): 8 - 12 . 21248475 DOI: 10.4161/psb.6.1.14012 http://doi.org/10.4161/psb.6.1.14012 . Cross-talk of calcium-dependent protein kinase and MAP kinase signaling Y Xiang , YH Lu , M Song , 等 . Overexpression of a Triticum aestivum calreticulin gene ( TaCRT1 ) improves salinity tolerance in tobacco . PLoS ONE , 2015 . 10 ( 10 ): e0140591 26469859 DOI: 10.1371/journal.pone.0140591 http://doi.org/10.1371/journal.pone.0140591 . Overexpression of a Triticum aestivum calreticulin gene (TaCRT1) improves salinity tolerance in tobacco HY Xiong , JJ Li , PL Liu , 等 . Overexpression of OsMYB48-1 , a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice . PLoS ONE , 2014 . 9 ( 3 ): e92913 24667379 DOI: 10.1371/journal.pone.0092913 http://doi.org/10.1371/journal.pone.0092913 . Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice LM Xiong , JK Zhu . Abiotic stress signal transduction in plants: molecular and genetic perspectives . Physiol Plant , 2001 . 112 ( 2 ): 152 - 166 . 11454221 DOI: 10.1034/j.1399-3054.2001.1120202.x http://doi.org/10.1034/j.1399-3054.2001.1120202.x . Abiotic stress signal transduction in plants: molecular and genetic perspectives LZ Xiong , YN Yang . Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase . Plant Cell , 2003 . 15 ( 3 ): 745 - 759 . 12615946 DOI: 10.1105/tpc.008714 http://doi.org/10.1105/tpc.008714 . Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase Q Xu , TT Truong , JM Barrero , 等 . A role for jasmonates in the release of dormancy by cold stratification in wheat . J Exp Bot , 2016 . 67 ( 11 ): 3497 - 3508 . 27140440 DOI: 10.1093/jxb/erw172 http://doi.org/10.1093/jxb/erw172 . A role for jasmonates in the release of dormancy by cold stratification in wheat ZS Xu , ZY Ni , L Liu , 等 . Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat . Mol Genet Genomics , 2008 . 280 ( 6 ): 497 - 508 . 18800227 DOI: 10.1007/s00438-008-0382-x http://doi.org/10.1007/s00438-008-0382-x . Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat ZS Xu , M Chen , LC Li , 等 . Functions of the ERF transcription factor family in plants . Botany , 2008 . 86 ( 9 ): 969 - 977 . DOI: 10.1139/B08-041 http://doi.org/10.1139/B08-041 . Functions of the ERF transcription factor family in plants ZS Xu , ZY Ni , ZY Li , 等 . Isolation and functional characterization of HvDREB1 –a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare . J Plant Res , 2009 . 122 ( 1 ): 121 - 130 . 19067111 DOI: 10.1007/s10265-008-0195-3 http://doi.org/10.1007/s10265-008-0195-3 . Isolation and functional characterization of HvDREB1–a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare DW Xue , YZ Huang , XQ Zhang , 等 . Identification of QTLs associated with salinity tolerance at late growth stage in barley . Euphytica , 2009 . 169 ( 2 ): 187 - 196 . DOI: 10.1007/s10681-009-9919-2 http://doi.org/10.1007/s10681-009-9919-2 . Identification of QTLs associated with salinity tolerance at late growth stage in barley GP Xue , CW Loveridge . HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element . Plant J , 2004 . 37 ( 3 ): 326 - 339 . 14731254 DOI: 10.1046/j.1365-313X.2003.01963.x http://doi.org/10.1046/j.1365-313X.2003.01963.x . HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element ZY Xue , DY Zhi , GP Xue , 等 . Enhanced salt tolerance of transgenic wheat ( Tritivum aestivum L.) expressing a vacuolar Na + /H + antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na + . Plant Sci , 2004 . 167 ( 4 ): 849 - 859 . DOI: 10.1016/j.plantsci.2004.05.034 http://doi.org/10.1016/j.plantsci.2004.05.034 . Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+ D Yadav , I Ahmed , P Shukla , 等 . Overexpression of Arabidopsis AnnAt8 alleviates abiotic stress in transgenic Arabidopsis and tobacco . Plants , 2016 . 5 ( 2 ): 18 DOI: 10.3390/plants5020018 http://doi.org/10.3390/plants5020018 . Overexpression of Arabidopsis AnnAt8 alleviates abiotic stress in transgenic Arabidopsis and tobacco C Yang , TJ Zhao , DY Yu , 等 . Isolation and functional characterization of a SERK gene from soybean ( Glycine max (L.) Merr.) . Plant Mol Biol Rep , 2011 . 29 ( 2 ): 334 - 344 . DOI: 10.1007/s11105-010-0235-8 http://doi.org/10.1007/s11105-010-0235-8 . Isolation and functional characterization of a SERK gene from soybean (Glycine max (L.) Merr.) SF Yang , NE Hoffman . Ethylene biosynthesis and its regulation in higher plants . Ann Rev Plant Physiol , 1984 . 35 155 - 189 . DOI: 10.1146/annurev.pp.35.060184.001103 http://doi.org/10.1146/annurev.pp.35.060184.001103 . Ethylene biosynthesis and its regulation in higher plants R Yarra . The wheat NHX gene family: potential role in improving salinity stress tolerance of plants . Plant Gene, 18:100178 , 2019 . DOI: 10.1016/j.plgene.2019.100178 http://doi.org/10.1016/j.plgene.2019.100178 . The wheat NHX gene family: potential role in improving salinity stress tolerance of plants R Yarra , PB Kirti . Expressing class I wheat NHX ( TaNHX2 ) gene in eggplant ( Solanum melongena L.) improves plant performance under saline condition . Funct Integr Genomics , 2019 . 19 ( 4 ): 541 - 554 . 30673892 DOI: 10.1007/s10142-019-00656-5 http://doi.org/10.1007/s10142-019-00656-5 . Expressing class I wheat NHX (TaNHX2) gene in eggplant (Solanum melongena L.) improves plant performance under saline condition HE Yen , SM Wu , YH Hung , 等 . Isolation of 3 salt-induced low-abundance cDNAs from light-grown callus of Mesembryanthemum crystallinum by suppression subtractive hybridization . Physiol Plant , 2000 . 110 ( 3 ): 402 - 409 . DOI: 10.1111/j.1399-3054.2000.1100315.x http://doi.org/10.1111/j.1399-3054.2000.1100315.x . Isolation of 3 salt-induced low-abundance cDNAs from light-grown callus of Mesembryanthemum crystallinum by suppression subtractive hybridization SY Yi , JH Kim , YH Joung , 等 . The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis . Plant Physiol , 2004 . 136 ( 1 ): 2862 - 2874 . 15347795 DOI: 10.1104/pp.104.042903 http://doi.org/10.1104/pp.104.042903 . The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis SY Yin , Y Han , L Huang , 等 . Overexpression of HvCBF7 and HvCBF9 changes salt and drought tolerance in Arabidopsis . Plant Growth Regul , 2018 . 85 ( 2 ): 281 - 292 . DOI: 10.1007/s10725-018-0394-4 http://doi.org/10.1007/s10725-018-0394-4 . Overexpression of HvCBF7 and HvCBF9 changes salt and drought tolerance in Arabidopsis XY Yin , AF Yang , KW Zhang , 等 . Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene . Acta Bot Sin-Engl Ed , 2004 . 46 ( 7 ): 854 - 861 . . Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene S Yousefirad , H Soltanloo , SS Ramezanpour , 等 . Salt oversensitivity derived from mutation breeding improves salinity tolerance in barley via ion homeostasis . Biol Plant , 2018 . 62 ( 4 ): 775 - 785 . DOI: 10.1007/s10535-018-0823-2 http://doi.org/10.1007/s10535-018-0823-2 . Salt oversensitivity derived from mutation breeding improves salinity tolerance in barley via ion homeostasis DD Zang , HY Li , HY Xu , 等 . An Arabidopsis zinc finger protein increases abiotic stress tolerance by regulating sodium and potassium homeostasis, reactive oxygen species scavenging and osmotic potential . Front Plant Sci, 7:1272 , 2016 . DOI: 10.3389/fpls.2016.01272 http://doi.org/10.3389/fpls.2016.01272 . An Arabidopsis zinc finger protein increases abiotic stress tolerance by regulating sodium and potassium homeostasis, reactive oxygen species scavenging and osmotic potential R Zardoya , XD Ding , Y Kitagawa , 等 . Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment . Proc Natl Acad Sci USA , 2002 . 99 ( 23 ): 14893 - 14896 . DOI: 10.1073/pnas.192573799 http://doi.org/10.1073/pnas.192573799 . Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment D Zhang , S Jiang , J Pan , 等 . The overexpression of a maize mitogen-activated protein kinase gene ( ZmMPK5 ) confers salt stress tolerance and induces defence responses in tobacco . Plant Biol , 2014 . 16 ( 3 ): 558 - 570 . 23952812 DOI: 10.1111/plb.12084 http://doi.org/10.1111/plb.12084 . The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco GQ Zhang , M Zhang , ZX Zhao , 等 . Wheat TaPUB1 modulates plant drought stress resistance by improving antioxidant capability . Sci Rep, 7:7549 , 2017 . DOI: 10.1038/s41598-017-08181-w http://doi.org/10.1038/s41598-017-08181-w . Wheat TaPUB1 modulates plant drought stress resistance by improving antioxidant capability HW Zhang , ZJ Huang , BY Xie , 等 . The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco . Planta , 2004 . 220 ( 2 ): 262 - 270 . 15300440 DOI: 10.1007/s00425-004-1347-x http://doi.org/10.1007/s00425-004-1347-x . The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco HX Zhang , LJ Irving , C McGill , 等 . The effects of salinity and osmotic stress on barley germination rate: sodium as an osmotic regulator . Ann Bot , 2010 . 106 ( 6 ): 1027 - 1035 . 20929898 DOI: 10.1093/aob/mcq204 http://doi.org/10.1093/aob/mcq204 . The effects of salinity and osmotic stress on barley germination rate: sodium as an osmotic regulator X Zhang , HW Ju , MS Chung , 等 . The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis . Plant Cell Physiol , 2011 . 52 ( 1 ): 138 - 148 . 21097474 DOI: 10.1093/pcp/pcq180 http://doi.org/10.1093/pcp/pcq180 . The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis XX Zhang , SK Liu , T Takano . Two cysteine proteinase inhibitors from Arabidopsis thaliana , AtCYSa and AtCYSb , increasing the salt, drought, oxidation and cold tolerance . Plant Mol Biol , 2008 . 68 ( 1-2 ): 131 - 143 . 18523728 DOI: 10.1007/s11103-008-9357-x http://doi.org/10.1007/s11103-008-9357-x . Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance XX Zhang , YJ Tang , QB Ma , 等 . OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean . PLoS ONE , 2013 . 8 ( 12 ): e83011 24376625 DOI: 10.1371/journal.pone.0083011 http://doi.org/10.1371/journal.pone.0083011 . OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean Y Zhang , C Chen , XF Jin , 等 . Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis . BMB Rep , 2009 . 42 ( 8 ): 486 - 492 . 19712584 DOI: 10.5483/bmbrep.2009.42.8.486 http://doi.org/10.5483/bmbrep.2009.42.8.486 . Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis YY Zhang , LL Wang , YL Liu , 等 . Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na + /H + antiport in the tonoplast . Planta , 2006 . 224 ( 3 ): 545 - 555 . 16501990 DOI: 10.1007/s00425-006-0242-z http://doi.org/10.1007/s00425-006-0242-z . Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast LQ Zhao , F Zhang , JK Guo , 等 . Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed . Plant Physiol , 2004 . 134 ( 2 ): 849 - 857 . 14739346 DOI: 10.1104/pp.103.030023 http://doi.org/10.1104/pp.103.030023 . Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed Y Zhao , XJ Tian , YY Li , 等 . Molecular and functional characterization of wheat ARGOS genes influencing plant growth and stress tolerance . Front Plant Sci, 8:170 , 2017 . DOI: 10.3389/fpls.2017.00170 http://doi.org/10.3389/fpls.2017.00170 . Molecular and functional characterization of wheat ARGOS genes influencing plant growth and stress tolerance JH Zhu , HZ Shi , BH Lee , 等 . An Arabidopsis homeodomain transcription factor gene, HOS9 , mediates cold tolerance through a CBF-independent pathway . Proc Natl Acad Sci USA , 2004 . 101 ( 26 ): 9873 - 9878 . DOI: 10.1073/pnas.0403166101 http://doi.org/10.1073/pnas.0403166101 . An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway JH Zhu , PE Verslues , XW Zheng , 等 . HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants . Proc Natl Acad Sci USA , 2005 . 102 ( 28 ): 9966 - 9971 . DOI: 10.1073/pnas.0503960102 http://doi.org/10.1073/pnas.0503960102 . HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants JK Zhu . Plant salt tolerance . Trends Plant Sci , 2001 . 6 ( 2 ): 66 - 71 . 11173290 DOI: 10.1016/S1360-1385(00)01838-0 http://doi.org/10.1016/S1360-1385(00)01838-0 . Plant salt tolerance JK Zhu . Salt and drought stress signal transduction in plants . Annu Rev Plant Biol , 2002 . 53 247 - 273 . 12221975 DOI: 10.1146/annurev.arplant.53.091401.143329 http://doi.org/10.1146/annurev.arplant.53.091401.143329 . Salt and drought stress signal transduction in plants JK Zhu . Regulation of ion homeostasis under salt stress . Curr Opin Plant Biol , 2003 . 6 ( 5 ): 441 - 445 . 12972044 DOI: 10.1016/S1369-5266(03)00085-2 http://doi.org/10.1016/S1369-5266(03)00085-2 . Regulation of ion homeostasis under salt stress JK Zhu , PM Hasegawa , RA Bressan , 等 . Molecular aspects of osmotic stress in plants . Crit Rev Plant Sci , 1997 . 16 ( 3 ): 253 - 277 . DOI: 10.1080/07352689709701950 http://doi.org/10.1080/07352689709701950 . Molecular aspects of osmotic stress in plants The authors would like to appreciate the expertise assistance from the institution and staff of Murdoch University, Western Barley Genetics Alliance, Western Australian State Agricultural Biotechnology Centre and the Department of Primary Industries and Regional Development (Australia). We are grateful to Peng-hao WANG and Yong JIA (Murdoch University, Australia) for their input during information analysis and cherish Le XU (Yangtze University, China) for comments on the manuscript and discussion. Compliance with ethics guidelines Edward MWANDO, Tefera Tolera ANGESSA, Yong HAN, and Chengdao LI declare that they have no conflict of interest. This article does not contain any studies with human or animal subjects performed by any of the authors. 10.1631/jzus.B1900400 ,, 2019-06-22 2019-09-25 2022-01-05 Copyright © Zhejiang University and Springer-Verlag GmbH Germany, part of Springer Nature 2020 2020 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 02 21