Effect of calcium and light on the germination of Urochondra setulosa under different salts

Effect of calcium and light on the germination of Urochondra setulosa under different salts 1 first-author 1 2 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:liweiq59@hotmail.com †E-mail:liweiq59@hotmail.com liweiq59@hotmail.com 2 1 Department of Botany, University of Karachi, Karachi 75270, Pakistan Department of Botany, University of Karachi, Karachi 75270, Pakistan Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang 050021, China Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang 050021, China Urochondra setulosa (Trin.) C.E. Hubbard is a coastal halophytic grass thriving on the coastal dunes along the Pakistani seashore. This grass could be useful in coastal sand dune stabilization using seawater irrigation. The purpose of this investigation was to test the hypothesis that Ca 2+ (0.0, 2.5, 5.0, 10.0 and 50.0 mmol/L) alleviates the adverse effects of KCl, MgSO 4 , NaCl and Na 2 SO 4 at 0, 200, 400, 600, 800 and 1000 mmol/L on the germination of Urochondra setulosa . Seed germination was inhibited with increase in salt concentration with few seeds germinated at and above 400 mmol/L concentration. No seed germinated in any of the KCl treatments. Inclusion of CaCl 2 substantially alleviated the inhibitory effects of all salts. Germination was higher under photoperiod in comparison to those seeds germinated under complete darkness. Among the CaCl 2 concentrations used, 10 mmol/L was most effective in alleviating salinity effects and allowing few seeds to germinate at 1000 mmol/L KCl, MgSO 4 , NaCl and Na 2 SO 4 solution. Calcium Germination KCl MgSO 4 NaCl Na 2 SO 4 Urochondra setulosa INTRODUCTION 1 Seed germination and seedling emergence are critical to the survival of plants in salt-affected areas (Khan, 2002 2002 ). Seeds of halophytes often germinate best under non-saline conditions with their germination decreasing with increasing salinity (Ungar, 1995 1995 ; Khan and Gul, 1998 1998 ; Khan, 2002 2002 ). Halophytic grasses that dominate the region have shown variable response to NaCl tolerance during germination (Khan and Gulzar, 2003 2003 ). Halopyrum mucronatum failed to germinate at or above 300 mmol/L NaCl (Khan and Ungar, 2001 2001 ) while Aeluropus lagopoides (Linn.) Trin. ex Thw., Sporobolus ioclados (Nees ex Trin.) Nees and Urochondra setulosa (Trin.) C.E. Hubbard could germinate in up to 500 mmol/L NaCl approaching seawater salinity (Khan and Gulzar, 2003 2003 ). Seed germination was almost completely inhibited in the absence of light for Sporobolus indicus (L.) R. Br. (Andrews, 1997 1997 ) and Triglochin maritima L. (Khan and Ungar, 1999 1999 ) and partially inhibited germination in Apium graveolens L. (Garcia et al., 1995 1995 ), Allium staticiforme Sibth. & Sm., Brassica tournefortii Gouan, Cakile maritima Scop., Onanthus maritimus (L.) Hoffmanns & Link (Thanos et al., 1991 1991 ) and Limonium stocksii (Zia and Khan, 2004 2004 ) while germination of seeds of Atriplex stocksii Boiss. (Khan and Rizvi, 1994 1994 ; Khan and Ungar, 2000 2000 ) and Suaeda fruticosa (Khan and Ungar, 1998 1998 ) was not inhibited by the absence of light. However, little information is available on the effect of Ca 2+ in improving seed germination under saline conditions. Saline soils are formed from the accumulation of various chloride and sulfate salts dominated by NaCl. The main salt components in saline soils are Na + , Mg 2+ and Ca 2+ cations and Cl − and SO 4 2− anions (Shainberg, 1975 1975 ). Only few studies (Hardegree and Emmerich, 1990 1990 ; Mohammad and Sen, 1990 1990 ; Egan et al., 1997 1997 ; Agboola, 1998 1998 ; Pujol et al., 2000 2000 ; Tobe et al., 2002 2002 ; Joshi et al., 2005 2005 ) have compared the effects of various salts on the germination of plants. Some studies indicated an osmotic effect of various chloride and sulfate salts on the germination but no specific ion effect (Mohammad and Sen, 1990 1990 ; Egan et al., 1997 1997 ; Agboola, 1998 1998 ; Pujol et al., 2000 2000 ) while others indicated both osmotic and ionic effects (Mohammad and Sen, 1990 1990 ; Duan et al., 2004 2004 ; Song et al., 2005 2005 ). Calcium alleviates the adverse effects of salinity in some plant species (Rengel, 1992 1992 ; Marschner, 1995 1995 ; Ebert et al., 2002 2002 ; Munns, 2002 2002 ; Bonilla et al., 2004 2004 ) and promotes plant growth (LaHaye and Epstein, 1969 1969 ; Cramer et al., 1986 1986 ; Kurth et al., 1986 1986 ; Suhayda et al., 1992 1992 ; Colmer et al., 1996 1996 ; Kinraide, 1999 1999 ) and alleviates the toxic effects of Na + and Mg 2+ on the germination of Kalidum caspicum (Tobe et al., 1999 1999 ; 2001 2001 ), pea (Bonilla et al., 2004 2004 ) and Hordeum vulgare (Bliss et al., 1986 1986 ). Tobe et al.( 2002 2002 ; 2004 2004 ) showed that Ca 2+ successfully alleviated the toxicity of various chloride and sulfate salts on the germination or seedling growth of Kalidium capsicum and Haloxylon ammodendron at relatively low concentration, and reduced K + outflux from seedlings, but caused no appreciable decrease in the influx of Na + or Mg 2+ into seedlings. The implication of the effects of calcium present in saline soil is far from clear. The establishment of U . setulosa in highly salinized areas is probably facilitated by the alleviation of salt toxicity to its radicles by the Ca 2+ present in the alkaline soils of these regions. This could result in increasing use of Ca 2+ as soil supplement to improve seed emergence. The present study was done to test the hypothesis that the application of calcium could successfully alleviate the inhibitory effect of chloride and sulfate salts on the seed germination of Urochondra setulosa . MATERIALS AND METHODS 1 Seeds of Urochondra setulosa were collected in 2002 from a salt flat located at Hawkes Bay near the Karachi coast. Tetrazolium test showed 100% viability in seeds. Seeds were surface sterilized with 1% sodium hypochlorite solution with germination experiment being started immediately. Germination was carried out in 50 mm×9 mm (Gelman No. 7232) tight-fitting plastic Petri dishes with 5 ml of test solution (0, 200, 400, 600, 800 and 1000 mmol/L NaCl, Na 2 SO 4 , MgSO 4 and KCl). Calcium chloride (0.0, 2.5, 5.0, 10.0 and 50.0 mmol/L) was also applied in addition to these salts. Four replicates of 25 seeds each were used for each treatment. Germination experiment was carried out at 20 °C:30 °C temperature regimes with a 12-h dark:light photoperiod (Sylvania cool white light, 110 μmol photons, m −2 ∙s −1 ). Germination was recorded every other day. Germination was also studied in 24 h darkness by placing the sets of Petri dishes in black bags at 20~30 °C. The germination in darkness was recorded on the 20th day of the experiment. Seeds were considered to be germinated with the emergence of the radical. The rate of germination was estimated by using a modified Timson index of germination velocity=∑ G / t , where G is the percent germination after 20 d and t is the total time of germination (Khan and Ungar, 1984 1984 ). Statistical analysis was carried out using SPSS ver. 9.0 (1999). RESULTS 1 A three-way ANOVA indicated significant ( F =309.8, P < 0.001) effect of calcium in alleviating germination-inhibiting effects of various salts ( F =46.8, P < 0.001), their concentrations ( F =2417.9, P < 0.001) and all significant interaction ( P < 0.001) on the germination of Urochondra setulosa seeds (Table 1 1 ). Maximum seed germination was obtained in non-saline control (Fig. 1 1 ). Addition of NaCl inhibited seed germination with few seeds germinated at 400 mmol/L NaCl (Fig. 1 1 ). NaCl and darkness had synergistic effect in inhibiting seed germination. Calcium (CaCl 2 ) alleviated seed germination when included in the growth medium with NaCl (Fig. 1 1 ). The CaCl 2 concentration of 10 mmol/L appeared to be optimal while few seeds germinated at 1000 mmol/L NaCl. Germination in darkness was significantly lower in all treatments in comparison to photoperiod (Fig. 1 1 ). Sources Sum of squares df Mean square F Significance Calcium 74603.333 4 18650.833 4.719 0.006 Salts 10222.400 4 2555.600 1.288 0.308 Salinity 549490.466 5 109898.093 26.863 0.000 Calcium×salts 12052.133 12 1004.344 2.003 0.040 Calcium×salinity 68984.267 20 3449.213 6.878 0.000 Salts×salinity 29624.400 20 1481.220 2.954 0.001 Calcium×salts×salinity 30089.867 60 501.498 9.359 0.000 Bar represents mean± SDE . Bonferroni letter represents significant difference ( P < 0.05) between salt treatments Effect of sodium sulfate on seed germination and its reversal by CaCl 2 showed a similar response as that of NaCl (Fig. 2 2 ). In the case of magnesium sulfate, 50 mmol/L CaCl 2 completely alleviated MgSO 4 effect in up to 600 mmol/L and 10 mmol/L CaCl 2 promoted more than 50% seed germination at 800 mmol/L MgSO 4 (Fig. 3 3 ). Potassium chloride was very toxic to germination and no seed germinated at 200 mmol/L KCl treatment (Fig. 4 4 ). Inclusion of CaCl 2 , however, substantially alleviated the adverse KCl effect on seed germination. Application of CaCl 2 (50 mmol/L) completely alleviated the 600 mmol/L KCl effect on seed germination (Fig. 4 4 ). Bar represents mean± SDE . Bonferroni letter represents significant difference ( P < 0.05) between salt treatments Bar represents mean± SDE . Bonferroni letter represents significant difference ( P < 0.05) between salt treatments Bar represents mean± SDE . Bonferroni letter represents significant difference ( P < 0.05) between salt treatments Rate of germination decreases with increase of concentrations in all salts (Tables 2 2 ~ 5 5 ). CaCl 2 (10.0 mmol/L) had higher rate of germination in comparison to distilled water control. When seed germinated in NaCl, rate of germination was highest when 10 mmol/L CaCl 2 was included (Table 2 2 ). Similar trend was noted with the treatment of sodium sulfate, potassium chloride and magnesium sulfate salts (Tables 3 3 ~ 5 5 ). CaCl 2 at higher concentration increased rate of germination more in MgSO 4 , followed by KCl, Na 2 SO 4 and NaCl (Tables 2 2 ~ 5 5 ). 3 NaCl (mmol/L) 5 Rate of germination 5 CaCl 2 (mmol/L) 0 2.5 5 10 50 0 34.3±1.9 41.0±1.4 35.2±1.5 43.2±0.4 36.4±0.1 200 27.3±2.2 36.1±1.1 40.2±0.8 41.6±1.1 36.7±1.0 400 0.2±0.2 23.0±3.1 29.1±3.2 36.7±2.0 27.5±1.1 600 0.0±0.0 2.4±0.6 5.5±0.7 13.7±2.1 0.7±0.3 800 0.0±0.0 0.1±0.1 0.3±0.3 1.1±0.6 0.0±0.0 1000 0.0±0.0 0.0±0.0 0.0±0.0 0.3±0.2 0.0±0.0 3 Na 2 SO 4 (mmol/L) 5 Rate of germination 5 CaCl 2 (mmol/L) 0 2.5 5 10 50 0 38.7±1.2 40.3±0.7 37.5±1.3 41.0±0.4 34.2±0.5 200 11.5±1.2 38.4±1.1 38.2±1.2 40.6±0.5 32.6±0.9 400 0.0±0.0 22.3±5.4 27.5±0.9 30.7±2.0 23.3±2.1 600 0.0±0.0 5.4±0.2 1.7±0.8 2.1±0.7 2.5±1.1 800 0.0±0.0 0.9±0.1 0.0±0.0 2.1±0.6 0.0±0.0 1000 0.0±0.0 0.4±0.4 0.0±0.0 0.2±0.2 0.0±0.0 3 KCl (mmol/L) 5 Rate of germination 5 CaCl 2 (mmol/L) 0 2.5 5 10 50 0 37.9±1.3 38.2±1.4 37.7±1.6 39.5±0.2 34.4±0.7 200 0.0±0.0 37.7±0.9 36.0±1.4 39.3±0.8 36.7±1.0 400 0.0±0.0 33.4±2.4 32.5±1.8 35.2±2.0 30.9±2.5 600 0.2±0.2 19.2±2.9 24.0±3.0 12.4±2.1 28.2±1.0 800 0.0±0.0 0.2±0.2 14.2±2.0 1.0±0.6 0.0±0.0 1000 0.0±0.0 0.0±0.0 0.0±0.0 0.4±0.4 0.0±0.0 3 MgSO 4 (mmol/L) 5 Rate of germination 5 CaCl 2 (mmol/L) 0 2.5 5 10 50 100 38.3±1.2 37.7±1.9 37.4±1.1 39.6±0.5 34.6±0.1 200 16.7±0.6 36.2±1.8 35.7±1.5 33.6±1.3 34.5±0.5 400 2.3±1.4 29.9±3.5 33.7±1.3 35.4±0.8 32.4±0.5 600 0.4±0.4 8.6±1.9 13.4±1.3 25.6±2.4 27.2±1.1 800 0.0±0.0 2.0±1.2 2.9±1.5 16.6±2.4 7.0±2.3 1000 0.0±0.0 0.5±0.3 0.0±0.0 3.0±1.2 0.6±0.6 DISCUSSION 1 Urochondra setulosa is a dominant species and one of the salt tolerant perennial grasses distributed in the coastal zone of Pakistan and forms hummocks on the farthest side of Pakistan’s Manora Creek which rarely gets inundated with seawater with plants probably surviving on oceanic seepage (Gulzar et al., 2001 2001 ; Khan and Gulzar, 2003 2003 ). Urochondra setulosa has erect and stout culms attaining a height of 15~90 cm, produces a large number of caryopses and also achieves vegetative reproduction by short rhizomes (Gulzar et al., 2001 2001 ). Other plants growing in association with U . setulosa include Limonium stocksii , Cyperus sp. in the drier zone and Arthrocnemum macrostachyum in the relatively wet low-lying zones. The grazing of the Urochondra setulosa population at Hawkes Bay by cattle indicates that this species could be used as a forage crop on saline soils (Gulzar et al., 2001 2001 ). Hawks Bay in Manora Creek also receives domestic and industrial wastes. The analyzed soil samples from the adjacent areas showed high concentrations of various sulfate and chloride ions. The base rock of the region is calcareous in nature with the amount of CaCO 3 in soil of this region being high. The area’s halophytes are reported to tolerate variable concentrations of NaCl during germination. They include Arthrocnemum macrostachyum (1000 mmol/L) (Khan and Gul, 1998 1998 ), Cressa cretica (800 mmol/L) (Khan, 1991 1991 ), Aeluropus lagopoides , Limonium stocksii , Sporobolus ioclados and Urochondra setulosa (500 mmol/L) (Khan and Gulzar, 2003 2003 ; Zia and Khan, 2004 2004 ), Halopyrum mucronatum (300 mmol/L) (Khan and Ungar, 2001 2001 ). Urochondra setulosa showed a similar response to MgCl 2 , KCl, and MgSO 4 , although KCl at lowest concentration (200 mmol/L) prevented any seed from germination. Ungar ( 1995 1995 ) reported that salt inhibition to halophyte Puccinellia festucaeformis was in the order CaCl 2 , MgCl 2 > NaCl, NaNO 3 , KCl > MgSO 4 . Several studies reported the effects of different salts common in the soil (Mohammad and Sen, 1990 1990 ; Egan et al., 1997 1997 ; Tobe et al., 2002 2002 ; Duan et al., 2004 2004 ). Most studies showed that the effect of salts on the germination is primarily osmotic and few researchers believed that it could be both ionic and osmotic (Mohammad and Sen, 1990 1990 ; Duan et al., 2004 2004 ; Joshi et al., 2005 2005 ; Song et al., 2005 2005 ). It appears that U . setulosa shows both osmotic and ionic effects, for example, KCl appears highly toxic, MgSO 4 less toxic. Our results for U . setulosa showed alleviation of the injurious effects of all salts with the application of CaCl 2 . This alleviating effect was more obvious on the seeds during the photoperiod compared to darkness germinated seeds. Tobe et al.( 2002 2002 ) also showed that calcium alleviated the adverse effects of NaCl, Na 2 SO 4 , MgCl 2 and PEG on the germination of Kalidium capsicum , indicating that the toxicity of different salts to radicles originates from a common mechanism. They attributed this CaCl 2 inhibition to an osmotic effect, which prevents radicle elongation. Other studies had different results, some showed little ameliorative effects (Leidi et al., 1991 1991 ) while other showed significant calcium effect in alleviating salinity stress on germination (Bliss et al., 1986 1986 ; Tobe et al., 2002 2002 ). The role of calcium in alleviating the adverse effect of NaCl and other salts on plant species (Rengel, 1992 1992 ; Marschner, 1995 1995 ; Girija et al., 2002 2002 ; Munns, 2002 2002 ; Tobe et al., 2002 2002 ) is not very well known. Experimental evidence implicates Ca 2+ function in salt adaptation (Parida and Das, 2005 2005 ). Externally supplied Ca 2+ reduces the toxic effects of NaCl, presumably by facilitating higher K + /Na + selectivity (Läuchli and Schubert, 1989 1989 ; Liu and Zhu, 1998 1998 ). High salinity also results in increased cytosolic Ca 2+ that is transported from the apoplast and intracellular compartments (Knight et al., 1997 1997 ). The resultant transient Ca 2+ increases potential stress signal transduction and leads to salt adaptation (Mendoza et al., 1994 1994 ; Knight et al., 1997 1997 ). A prolonged elevated Ca 2+ level may, however, also pose a stress; if so, reestablishment of Ca 2+ homeostasis is a requisite (Parida and Das, 2005 2005 ). The changes in [Ca 2+ ] Cyt perturbations following combinations of oxidative stress and hyper-osmotic stress correlated well with the expression of Ca 2+ -regulated osmotic stress induced genes, and the acquisition of osmotic stress tolerance (Knight et al., 1998 1998 ). More research on Ca 2+ in plants has been focused at the cellular level due to realization that [Ca 2+ ] Cyt is an obligate intracellular messenger coordinating the cellular responses to numerous developmental cues and environmental challenges (White and Broadley, 2003 2003 ; Plieth, 2005 2005 ). Little information is available on enhancing seed germination in darkness by the application of CaCl 2 . 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