Effects of exogenous application of abscisic acid on membrane stability, osmotic adjustment, photosynthesis and hormonal status of two lucerne (Medicago sativa L.) genotypes under high temperature stress and drought stress
Yuan An A B C , Peng Zhou A and Jinfeng Liang A
+ Author Affiliations
- Author Affiliations
A College of Agriculture and Biology, Shanghai Jiaotong University, Shanghai 201101, P.R. China.
B Key Laboratory of Urban Agriculture (South), Ministry of Agriculture, Shanghai, 201101, P.R. China.
C Corresponding author. Email: anyuan@sjtu.edu.cn
Crop and Pasture Science 65(3) 274-286 https://doi.org/10.1071/CP13162
Submitted: 8 May 2013 Accepted: 11 January 2014 Published: 4 April 2014
Abstract
This study was designed to examine effects of high temperature, drought and exogenous abscisic acid (ABA) on membrane stability, osmotic adjustment, photosynthesis and the hormone status of two lucerne (alfalfa, Medicago sativa L.) genotypes contrasting in heat tolerance: Ameristand 801S (AS801) (heat-tolerant), and Aohan (heat-sensitive), The results showed that AS801 had lower electrolyte leakage, but higher chlorophyll content, net photosynthetic rate, stomatal conductance, proline content, ABA content and zeatin riboside (ZR) content than Aohan during 72 h of heat stress under well-watered conditions. Under drought conditions, however, only proline content and ZR content in roots, electrolyte leakage in leaves and roots, net photosynthetic rate, and ABA content were significantly different between the two genotypes. A foliar application of ABA to heat-stressed plants significantly decreased electrolyte leakage and stomatal conductance, and increased recovery in growth and leaf water potential in the two genotypes under both watering conditions. The other physiological responses measured differed under drought or well-watered conditions, and appeared to be genotype-specific. These results suggest that the physiological responses of heat-sensitive and heat-tolerant lucerne to heat stress under different soil-water conditions varied. The heat-induced changes in proline accumulation in roots, electrolyte leakage in leaves and roots, and photosynthetic rate could serve as early instant stress indicators for evaluating the tolerance of lucerne genotypes to heat stress under different soil water conditions.
Additional keywords: abscisic acid, alfalfa, drought high temperature.
References
Alves AAC, Setter TL (2004) Abscisic acid accumulation and osmotic adjustment in cassava under water deficit. Environmental and Experimental Botany 51, 259–271.| Abscisic acid accumulation and osmotic adjustment in cassava under water deficit.Crossref | GoogleScholarGoogle Scholar |
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.
| Drought and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Bates LS (1973) Rapid determination of free proline for water stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for water stress studies.Crossref | GoogleScholarGoogle Scholar |
Bollmark M, Kubat B, Eliasson L (1988) Variations in endogenous cytokinin content during adventitious root formation in pea cuttings. Journal of Plant Physiology 132, 262–265.
| Variations in endogenous cytokinin content during adventitious root formation in pea cuttings.Crossref | GoogleScholarGoogle Scholar |
Camejo D, Rodríguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology 162, 281–289.
| High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility.Crossref | GoogleScholarGoogle Scholar | 15832680PubMed |
Chandrasekar V, Sairam RK, Srivastava GC (2000) Physiological and biochemical responses of hexaploid and tetraploid wheat to drought stress. Journal of Agronomy & Crop Science 191, 450–457.
Cvikrová M, Gemperlová L, Dobrá J, Martincová O, Prásil IT, Gubisc J, Vanková R (2012) Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Science 182, 49–58.
| Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants.Crossref | GoogleScholarGoogle Scholar | 22118615PubMed |
Dobra J, Motyka V, Dobrev P, Malbeck J, Prasil IT, Haisel D, Gaudinova A, Havlova M, Gubis J, Vankova R (2010) Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology 167, 1360–1370.
| Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content.Crossref | GoogleScholarGoogle Scholar | 20619485PubMed |
Evers D, Lefèvre I, Legay S, Lamoureux D, Hausman JF, Rosales ROG, Marca LRT, Hoffmann L, Bonierbale M, Schafleitner R (2010) Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. Journal of Experimental Botany 61, 2327–2343.
| Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach.Crossref | GoogleScholarGoogle Scholar | 20406784PubMed |
Gomes FP, Oliva MA, Mielke MS, Almeida AAF, Leite HG, Aquino LA (2009) Is abscisic acid involved in the drought responses of Brazilian Green Dwarf coconut? Experimental Agriculture 45, 189–198.
| Is abscisic acid involved in the drought responses of Brazilian Green Dwarf coconut?Crossref | GoogleScholarGoogle Scholar |
Gomes FP, Oliva MA, Mielke MS, Almeida AAF, Aquino LA (2010) Osmotic adjustment, proline accumulation and cell membrane stability in leaves of Cocos nucifera submitted to drought stress. Scientia Horticulturae 126, 379–384.
| Osmotic adjustment, proline accumulation and cell membrane stability in leaves of Cocos nucifera submitted to drought stress.Crossref | GoogleScholarGoogle Scholar |
Gong M, Li YJ, Chen SZ (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. Journal of Plant Physiology 153, 488–496.
| Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems.Crossref | GoogleScholarGoogle Scholar |
Guóth A, Tari I, Gallé Á, Csiszár J, Pécsváradi A, Cseuz L, Erdei L (2009) Comparison of the drought stress responses of tolerant and sensitive wheat cultivars during grain filling: changes in flag leaf photosynthetic activity, ABA levels, and grain yield. Journal of Plant Growth Regulation 28, 167–176.
| Comparison of the drought stress responses of tolerant and sensitive wheat cultivars during grain filling: changes in flag leaf photosynthetic activity, ABA levels, and grain yield.Crossref | GoogleScholarGoogle Scholar |
Haldimann P, Feller U (2004) Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant, Cell & Environment 27, 1169–1183.
| Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase.Crossref | GoogleScholarGoogle Scholar |
Hamerlynck EP, Huxman TE, Loik ME, Smith SD (2000) Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub, Larrea tridentate. Plant Ecology 148, 183–193.
| Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub, Larrea tridentate.Crossref | GoogleScholarGoogle Scholar |
Hassine AB, Lutts S (2010) Differential responses of saltbush Atriplex halimus L. exposed to salinity and water stress in relation to senescing hormones abscisic acid and ethylene. Journal of Plant Physiology 167, 1448–1456.
| Differential responses of saltbush Atriplex halimus L. exposed to salinity and water stress in relation to senescing hormones abscisic acid and ethylene.Crossref | GoogleScholarGoogle Scholar | 20869134PubMed |
Hu XL, Li YH, Li CH, Yang HR, Wang W, Lu MH (2010) Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress. Journal of Plant Growth Regulation 29, 455–464.
| Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress.Crossref | GoogleScholarGoogle Scholar |
Jia HS, Lu CM (2003) Effects of abscisic acid on photoinhibition in maize plants. Plant Science 165, 1403–1410.
| Effects of abscisic acid on photoinhibition in maize plants.Crossref | GoogleScholarGoogle Scholar |
Kavi KPB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Current Science 88, 424–438.
Knipp G, Honermeier B (2006) Effect of water stress on proline accumulation of genetically modified potatoes (Solanum tuberosum L.) generating fructans. Journal of Plant Physiology 163, 392–397.
| Effect of water stress on proline accumulation of genetically modified potatoes (Solanum tuberosum L.) generating fructans.Crossref | GoogleScholarGoogle Scholar | 16455352PubMed |
Kuznetsov VV, Rakitin VY, Zholkevich VN (1999) Effects of preliminary heat-shock treatment on accumulation of osmolytes and drought resistance in cotton plants during water deficiency. Physiologia Plantarum 107, 399–406.
| Effects of preliminary heat-shock treatment on accumulation of osmolytes and drought resistance in cotton plants during water deficiency.Crossref | GoogleScholarGoogle Scholar |
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128, 682–695.
| Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid.Crossref | GoogleScholarGoogle Scholar | 11842171PubMed |
Li HS (2000) ‘Principles and techniques of plant physiological experiment.’ pp. 134–136. (Higher Education Press: Beijing) [in Chinese]
Liu X, Huang B (2002) Cytokinin effects on creeping bentgrass response to heat stress. Part II. Leaf senescence and antioxidant metabolism. Crop Science 42, 466–472.
| Cytokinin effects on creeping bentgrass response to heat stress. Part II. Leaf senescence and antioxidant metabolism.Crossref | GoogleScholarGoogle Scholar |
Liu XZ, Huang BR (2005) Root physiological factors involved in cool-season grass response to high soil temperature. Environmental and Experimental Botany 53, 233–245.
| Root physiological factors involved in cool-season grass response to high soil temperature.Crossref | GoogleScholarGoogle Scholar |
Liu X, Huang H, Banowetz G (2002) Cytokinin effects on creeping bentgrass response to heat stress. I. Shoot and root growth. Crop Science 42, 457–465.
| Cytokinin effects on creeping bentgrass response to heat stress. I. Shoot and root growth.Crossref | GoogleScholarGoogle Scholar |
Lobell DB, Asner GP (2003) Climate and management contributions to recent trends in US agricultural yields. Science 299, 1032
| Climate and management contributions to recent trends in US agricultural yields.Crossref | GoogleScholarGoogle Scholar | 12586935PubMed |
Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany 78, 389–398.
| NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance.Crossref | GoogleScholarGoogle Scholar |
Machado S, Paulsen GM (2001) Combined effects of drought and high temperature on water relations of wheat and sorghum. Plant and Soil 233, 179–187.
| Combined effects of drought and high temperature on water relations of wheat and sorghum.Crossref | GoogleScholarGoogle Scholar |
Nayyar H, Walia DP (2004) Genotypic variation in wheat in response to water stress and abscisic acid-induced accumulation of osmolytes in developing grains. Journal of Agronomy & Crop Science 190, 39–45.
| Genotypic variation in wheat in response to water stress and abscisic acid-induced accumulation of osmolytes in developing grains.Crossref | GoogleScholarGoogle Scholar |
Ozfidan C, Turkan I, Sekmen AH, Seckin B (2013) Time course analysis of ABA and non-ionic osmotic stress-induced changes in water status, chlorophyll fluorescence and osmotic adjustment in Arabidopsis thaliana wild-type (Columbia) and ABA-deficient mutant (aba2). Environmental and Experimental Botany 86, 44–51.
| Time course analysis of ABA and non-ionic osmotic stress-induced changes in water status, chlorophyll fluorescence and osmotic adjustment in Arabidopsis thaliana wild-type (Columbia) and ABA-deficient mutant (aba2).Crossref | GoogleScholarGoogle Scholar |
Pospíšilová J, Batková P (2004) Effects of pre-treatments with abscisic acid and /or benzyladenine on gas exchange of French bean, sugar beet, and maize leaves during water stress and after rehydration. Biologia Plantarum 48, 395–399.
| Effects of pre-treatments with abscisic acid and /or benzyladenine on gas exchange of French bean, sugar beet, and maize leaves during water stress and after rehydration.Crossref | GoogleScholarGoogle Scholar |
Rai AC, Singh M, Shah K (2012) Effect of water withdrawal on formation of free radical, proline accumulation and activities of antioxidant enzymes in ZAT12-transformed transgenic tomato plants. Plant Physiology and Biochemistry 61, 108–114.
Rampino P, Mita G, Fasano P, Borrelli GM, Aprile A, Dalessandro G, Bellis LD, Perrotta C (2012) Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiology and Biochemistry 56, 72–78.
| Novel durum wheat genes up-regulated in response to a combination of heat and drought stress.Crossref | GoogleScholarGoogle Scholar | 22609457PubMed |
Reynolds-Henne CE, Langenegger A, Mani J, Schenk N, Zumsteg A, Feller U (2010) Interactions between temperature, drought and stomatal opening in legumes. Environmental and Experimental Botany 68, 37–43.
| Interactions between temperature, drought and stomatal opening in legumes.Crossref | GoogleScholarGoogle Scholar |
Sainz M, Díaz P, Monza J, Borsani O (2010) Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to Photosystem II in combined drought-heat stressed Lotus japonicus. Physiologia Plantarum 140, 46–56.
| Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to Photosystem II in combined drought-heat stressed Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 20487374PubMed |
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296–302.
| Regulatory metabolic networks in drought stress responses.Crossref | GoogleScholarGoogle Scholar | 17468040PubMed |
Setter TL, Flannigan BA, Melkonian J (2001) Loss of kernel set due to water deficit and shade in maize: carbohydrate supplies, abscisic acid, and cytokinins. Crop Science 41, 1530–1540.
| Loss of kernel set due to water deficit and shade in maize: carbohydrate supplies, abscisic acid, and cytokinins.Crossref | GoogleScholarGoogle Scholar |
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57, 711–726.
| The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress.Crossref | GoogleScholarGoogle Scholar | 16473893PubMed |
Sharp RE, LeNoble ME, Else MA, Eleanor TT, Gherardi F (2000) Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. Journal of Experimental Botany 51, 1575–1584.
| Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene.Crossref | GoogleScholarGoogle Scholar | 11006308PubMed |
Silva EN, Ferreira-Silva SL, Fontenelea AV, Ribeiro RV, Viégasc RA, Silveira JAG (2010) Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. Journal of Plant Physiology 167, 1157–1164.
| Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants.Crossref | GoogleScholarGoogle Scholar | 20417989PubMed |
Simon-Sarkadi L, Kocsy G, Várhegyi À, Galiba G, de Ronde JA (2005) Genetic manipulation of proline accumulation influences the concentrations of other amino acids in soybean subjected to simultaneous drought and heat stress. Journal of Agricultural and Food Chemistry 53, 7512–7517.
| Genetic manipulation of proline accumulation influences the concentrations of other amino acids in soybean subjected to simultaneous drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 16159180PubMed |
Singh B, Singh G (2006) Effects of controlled irrigation on water potential, nitrogen uptake and biomass production in Dalbergia sissoo seedlings. Environmental and Experimental Botany 55, 209–219.
| Effects of controlled irrigation on water potential, nitrogen uptake and biomass production in Dalbergia sissoo seedlings.Crossref | GoogleScholarGoogle Scholar |
Slama I, Messedi D, Ghnaya T, Savoure A, Abdelly C (2006) Effects of water deficit on growth and proline metabolism in Sesuvium portulacastrum. Environmental and Experimental Botany 56, 231–238.
| Effects of water deficit on growth and proline metabolism in Sesuvium portulacastrum.Crossref | GoogleScholarGoogle Scholar |
Song LL, Ding W, Shen J, Zhang ZG, Bi YR, Zhang LX (2008) Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Science 175, 826–832.
| Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress.Crossref | GoogleScholarGoogle Scholar |
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
| Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 20036181PubMed |
Travaglia C, Cohen AC, Reinoso H, Castillo C, Bottini R (2007) Exogenous abscisic acid increases carbohydrate accumulation and redistribution to the grains in wheat grown under field conditions of soil water restriction. Journal of Plant Growth Regulation 26, 285–289.
| Exogenous abscisic acid increases carbohydrate accumulation and redistribution to the grains in wheat grown under field conditions of soil water restriction.Crossref | GoogleScholarGoogle Scholar |
Trotel-Aziz P, Niogret MF, Larher F (2000) Proline level is partly under the control of abscisic acid in canola leaf discs during recovery from hyper-osmotic stress. Physiologia Plantarum 110, 376–383.
| Proline level is partly under the control of abscisic acid in canola leaf discs during recovery from hyper-osmotic stress.Crossref | GoogleScholarGoogle Scholar |
Trotel-Aziz P, Niogret MF, Deleu C, Bouchereau A, Aziz A, Larher FR (2003) The control of proline consumption by abscisic acid during osmotic stress recovery of canola leaf discs. Physiologia Plantarum 117, 213–221.
| The control of proline consumption by abscisic acid during osmotic stress recovery of canola leaf discs.Crossref | GoogleScholarGoogle Scholar |
Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology 164, 1367–1376.
| Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat.Crossref | GoogleScholarGoogle Scholar |
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35, 753–759.
Wahid A, Gelani S, Ashraf M, Foolad R (2007) Heat tolerance in plants: An overview. Environmental and Experimental Botany 61, 199–223.
| Heat tolerance in plants: An overview.Crossref | GoogleScholarGoogle Scholar |
Wang ZL, Mambelli S, Setter TL (2002) Abscisic acid catabolism in maize kernels in response to water deficit at early endosperm development. Annals of Botany 90, 623–630.
| Abscisic acid catabolism in maize kernels in response to water deficit at early endosperm development.Crossref | GoogleScholarGoogle Scholar |
Wilkinson S, Davies WJ (2002) ABA-based chemical signaling: the co-ordination of responses to stress in plants. Plant, Cell & Environment 25, 195–210.
| ABA-based chemical signaling: the co-ordination of responses to stress in plants.Crossref | GoogleScholarGoogle Scholar |
Wise RR, Olson AJ, Schrander SM, Scharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-frown Pima cotton plants at high temperature. Plant, Cell & Environment 27, 717–724.
| Electron transport is the functional limitation of photosynthesis in field-frown Pima cotton plants at high temperature.Crossref | GoogleScholarGoogle Scholar |
Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2003) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant, Cell & Environment 26, 1621–1631.
| Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling.Crossref | GoogleScholarGoogle Scholar |
Yang JC, Zhang JH, Ye YX, Wang ZQ, Zhu QS, Liu LJ (2004) Involvement of abscisic acid and ethylene in the responses of rice grains to water stress during filling. Plant, Cell & Environment 27, 1055–1064.
| Involvement of abscisic acid and ethylene in the responses of rice grains to water stress during filling.Crossref | GoogleScholarGoogle Scholar |
Yoshikawa H, Honda C, Kondo S (2007) Effect of low-temperature stress on abscisic acid, jasmonates, and polyamines in apples. Journal of Plant Growth Regulation 52, 199–206.
| Effect of low-temperature stress on abscisic acid, jasmonates, and polyamines in apples.Crossref | GoogleScholarGoogle Scholar |
Zhang CS, Lu G, Verma DPS (1997) Characterization of Δ1-pyrroliline-5-carboxylate synthetase, gene promoter in transgenic Arabidopsis thaliana subjected to water stress. Plant Science 129, 81–89.
| Characterization of Δ1-pyrroliline-5-carboxylate synthetase, gene promoter in transgenic Arabidopsis thaliana subjected to water stress.Crossref | GoogleScholarGoogle Scholar |
Zhang YM, Yang JF, Lu SY, Cai JL, Guo ZF (2008) Overexpressing SgNCED1 in tobacco increases ABA level, antioxidant enzyme activities, and stress tolerance. Journal of Plant Growth Regulation 27, 151–158.
| Overexpressing SgNCED1 in tobacco increases ABA level, antioxidant enzyme activities, and stress tolerance.Crossref | GoogleScholarGoogle Scholar |
