Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea
Rashmi Awasthi A , Neeru Kaushal A , Vincent Vadez B , Neil C. Turner C D , Jens Berger E , Kadambot H. M. Siddique D and Harsh Nayyar A FA Department of Botany, Panjab University, Chandigarh, 160014, India.
B International Crops Research Institute for Semiarid Tropics, Patancheru, 502 324 Andra Pradesh, India.
C Centre for Legumes in Mediterranean Agriculture, The University of Western Australia, Crawley, WA 6009, Australia.
D The Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia.
E CSIRO Plant Industry, Private Bag No. 5, Wembley, WA 6913, Australia.
F Corresponding author. Email: harshnayyar@hotmail.com
Functional Plant Biology 41(11) 1148-1167 https://doi.org/10.1071/FP13340
Submitted: 22 November 2013 Accepted: 23 April 2014 Published: 13 June 2014
Abstract
High temperatures and decreased rainfall are detrimental to yield in chickpea (Cicer arietinum L.), particularly during grain filling. This study aimed to (i) assess the individual and combined effects of drought and heat stress on biochemical seed-filling processes, (ii) determine genotypic differences in heat and drought tolerance, and (iii) determine any cross-tolerance. Plants were grown outdoors in the normal growing season when temperatures during seed filling were <32−20°C or were planted late (temperatures >32−20°C; heat stress). Half of the pots were kept adequately watered throughout, but water was withheld from the others from the initiation of seed filling until the relative leaf water content reached 50% of the irrigated plants (drought stress); all plants were rewatered thereafter until seed maturit. Water was withheld for 13 days (normal sowing) and 7 days (late sowing), so soil moisture decreased by 54–57%. Tests on leaves and seeds were performed after the stress. Individual and combined stress damaged membranes, and decreased cellular oxidising ability, stomatal conductance, PSII function and leaf chlorophyll content; damage was greater under combined stress. Leaf Rubisco activity increased with heat stress, decreased with drought stress and decreased severely with combined stress. Sucrose and starch concentrations decreased in all seeds through reductions in biosynthetic enzymes; reductions were greater under combined stress. These effects were more severe in heat- and drought-sensitive genotypes compared with drought-tolerant genotypes. Drought stress had a greater effect than heat stress on yield and the biochemical seed-filling mechanisms. Drought- and heat-tolerant genotypes showed partial cross-tolerance.
Additional keywords: Cicer arietinum, high temperature, seed yield, water stress.
References
Ahmadi A, Baker DA (2001) The effect of water stress on grain filling processes in wheat. The Journal of Agricultural Science 136, 257–269.| The effect of water stress on grain filling processes in wheat.Crossref | GoogleScholarGoogle Scholar |
Almeselmani M, Abdullah F, Hareri F, Naaesan M, Ammar MA, Kanbar OZ, Saud AA (2011) Effect of drought on different physiological characters and yield component in different varieties of syrian durum wheat. The Journal of Agricultural Science 3, 127–133.
Andersen MN, Asch F, Wu Y, Jensen CR, Næsted H, Mogensen VO, Koch KE (2002) Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiology 130, 591–604.
| Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKnt74%3D&md5=11579574bdcb100c6b4d68198bc1e5bbCAS | 12376627PubMed |
Anderson CM, Kohorn BD (2001) Inactivation of Arabidopsis SIP1 leads to reduced levels of sugars and drought tolerance. Journal of Plant Physiology 158, 1215–1219.
| Inactivation of Arabidopsis SIP1 leads to reduced levels of sugars and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVSqsLc%3D&md5=ba752052c649ddbe98ec66907785475fCAS |
Arnon DI (1949) Copper enzyme in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiology 24, 1–15.
| Copper enzyme in isolated chloroplasts: polyphenol oxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=994802752a64f327871eb14f54acacefCAS | 16654194PubMed |
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51, 163–190.
| Photosynthesis under stressful environments: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFeiu7s%3D&md5=4b77ba2adcce19ba536e128d04ac15b5CAS |
Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431, 181–184.
| Ecosystem stability and compensatory effects in the Inner Mongolia grassland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlGks7w%3D&md5=8ea05a2681efd9cff1a00a0e2fc81b8cCAS | 15356630PubMed |
Balla K, Rakszegi M, Li Z, Bekes F, Bencze S, Veisz O (2011) Quality of winter wheat in relation to heat and drought shock after anthesis. Czech Journal of Food Sciences 29, 117–128.
Barnabás B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell & Environment 31, 11–38.
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences 24, 519–570.
Basu PS, Berger JD, Turner NC, Chaturved SK, Ali M, Siddique KHM (2007) Osmotic adjustment of chickpea (Cicer arietinum) is not associated with changes in carbohydrate composition or leaf gas exchange under drought. Annals of Applied Biology 150, 217–225.
| Osmotic adjustment of chickpea (Cicer arietinum) is not associated with changes in carbohydrate composition or leaf gas exchange under drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVSnuro%3D&md5=9973af2d71f15c0a1f21f1698d72bbc5CAS |
Baun LC, Palmiano EP, Perez CM, Juliano BO (1970) Enzymes of starch metabolism in the developing rice grain. Plant Physiology 46, 429–434.
| Enzymes of starch metabolism in the developing rice grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXivVyntw%3D%3D&md5=1e596a2edf3892b78efbe0a91114c9beCAS | 16657480PubMed |
Behboudian MH, Ma Q, Turner NC, Palta JA (2001) Reactions of chickpea to water stress: yield and seed composition. Journal of the Science of Food and Agriculture 81, 1288–1291.
| Reactions of chickpea to water stress: yield and seed composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1Cntr0%3D&md5=641b33b9d8c90a414873ead582c0033cCAS |
Bhatt RM, Srinivasa Rao NK, Upreti KK, Shobha HS (2009) Floral abscission and changes in sucrose phosphate synthase and invertase activities in water deficient tomato. Indian Journal of Plant Physiology 4, 370–376.
Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytologist 162, 671–681.
| Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlyrsro%3D&md5=255f4a1c95870b56f35c584e6aacefd7CAS |
Cairns JE, Crossa J, Zaidi PH, Grudloyma P, Sanchez C, Araus JL, Thaitad S, Makumbi D, Magorokosho C, Banziger M, Menkir A, Hearne S, Atlin GN (2013) Identification of drought, heat and combined drought and heat tolerant donors in maize (Zea mays L). Crop Science
| Identification of drought, heat and combined drought and heat tolerant donors in maize (Zea mays L).Crossref | GoogleScholarGoogle Scholar |
Canci H, Toker C (2009) Evaluation of yield criteria for drought and heat resistance in chickpea (Cicer arietinum L). Journal Agronomy & Crop Science 195, 47–54.
| Evaluation of yield criteria for drought and heat resistance in chickpea (Cicer arietinum L).Crossref | GoogleScholarGoogle Scholar |
Carmo-Silva AE, Gore MA, Andrade-Sanchez P, French AN, Hunsaker DJ, Salvucci ME (2012) Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environmental and Experimental Botany 83, 1–11.
| Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvFOrsbw%3D&md5=6f75ad405a1ac3557996bd5e3a8751c6CAS |
Castrillo M (1992) Sucrose metabolism in bean plants under water deficit. Journal of Experimental Botany 43, 1557–1561.
| Sucrose metabolism in bean plants under water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVWgsQ%3D%3D&md5=d00ce347cb7f2fab876f9f4703b99e79CAS |
Chaitanya KV, Sundar D, Reddy AR (2001) Mulberry leaf metabolism under high temperature stress. Journal of Plant Biology 44, 379–384.
| Mulberry leaf metabolism under high temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtlentrs%3D&md5=ee5f61e30e6910c3b22c7d774fff3754CAS |
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Functional Plant Biology 30, 239–264.
| Understanding plant responses to drought – from genes to the whole plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKlt7o%3D&md5=308e85a17dc620123b40725d9fc5bb2eCAS |
Conde A, Chaves MM, Geros H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant & Cell Physiology 52, 1583–1602.
| Membrane transport, sensing and signaling in plant adaptation to environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1SiurvL&md5=5b4ccd4aa1807c2f967bfdd888763b52CAS |
Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In ‘Photosynthesis and the environment’. (Ed. NR Baker) pp. 347–366. (Kluwer Academic Publishers: New York)
Davies SL, Turner NC, Siddique KHM, Plummer JA, Leport L (1999) Seed growth of desi and kabuli chickpea types of chickpea exposed to terminal drought (Cicer arietinum L) in a short-season Mediterranean-type environment. Australian Journal of Experimental Agriculture 39, 181–188.
| Seed growth of desi and kabuli chickpea types of chickpea exposed to terminal drought (Cicer arietinum L) in a short-season Mediterranean-type environment.Crossref | GoogleScholarGoogle Scholar |
Dejardin A, Rochat C, Maugenest S, Boutin JP (1997) Purification, characterisation and physiological role of sucrose synthase in the pea sea coat (Pisum sativum L.). Planta 20, 128–137.
Deshmukh DV, Mate SN (2013) Evaluation of pigeonpea genotypes for morpho-physiological traits related to drought tolerance. World Journal of Agricultural Sciences 9, 17–23.
Devasirvatham V, Gaur PM, Mallikarjuna N, Tokachichu RN, Trethowan RM, Tan DKY (2012) Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. Functional Plant Biology 39, 1009–1018.
| Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments.Crossref | GoogleScholarGoogle Scholar |
Djanaguiraman M, Prasad PVV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiology and Biochemistry 48, 999–1007.
| Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKmsr%2FM&md5=00215f7e31d565fc1102479a8e1bd5afCAS | 20951054PubMed |
Earnshaw MJ (1993) Stress indicators: electrolyte leakage. In ‘Methods in comparative ecology’. (Eds GAF Hendry, JP Grime) pp. 152–154. (Chapman and Hall: London)
Egli DB, Bruening WP (2004) Water stress, photosynthesis, seed sucrose levels and seed growth in soybean. The Journal of Agricultural Science 142, 1–8.
| Water stress, photosynthesis, seed sucrose levels and seed growth in soybean.Crossref | GoogleScholarGoogle Scholar |
Faraji A, Latifi N, Soltani A, Rad AHS (2008) Effect of high temperature and supplemental irrigation in flower and pod formation in two canola (Brassica napus L) cultivar at Mediterranean climate. Asian Journal of Plant Science 7, 343–351.
| Effect of high temperature and supplemental irrigation in flower and pod formation in two canola (Brassica napus L) cultivar at Mediterranean climate.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=1b7b578571b22881f7134e65a1c8f68dCAS |
Fu J, Huang B, Fry J (2010) Osmotic potential, sucrose level, and activity of sucrose metabolic enzymes in tall fescue in response to deficient irrigation. Journal of the American Society for Horticultural Science 135, 506–510.
Hamidou F, Halilou O, Vadez V (2013) Assessment of groundnut under combined heat and drought Stress. Journal Agronomy & Crop Science 199, 1–11.
| Assessment of groundnut under combined heat and drought Stress.Crossref | GoogleScholarGoogle Scholar |
Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Annals of Botany 89, 851–859.
| Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitLg%3D&md5=ad0a2a63d6202e302c5c9c0cb22f4f54CAS | 12102511PubMed |
Havaux M (1992) Stress tolerance of Photosystem II in vivo antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiology 100, 424–432.
| Stress tolerance of Photosystem II in vivo antagonistic effects of water, heat, and photoinhibition stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgsbw%3D&md5=500ab1dc23af326376d0aa288db5b1f0CAS | 16652979PubMed |
Hawker JS, Jenner CJ (1993) High temperature affects the activity of enzymes in the committed pathway of starch synthesis in developing wheat endosperm. Australian Journal of Plant Physiology 20, 197–209.
| High temperature affects the activity of enzymes in the committed pathway of starch synthesis in developing wheat endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvFWgur4%3D&md5=91875dcaed51faef8ffb206b0d4d5efdCAS |
Hawker JS, Walker RR, Ruffner HP (1976) Invertase and sucrose synthase in flowers. Phytochemistry 15, 1441–1444.
| Invertase and sucrose synthase in flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlvVyht7k%3D&md5=d93a60c3485656ed840394ca8e22e9ffCAS |
Jacobsen JV, Hanson AD, Chandler PC (1986) Water stress enhances expression of an alpha-amylase gene in barley leaves. Plant Physiology 80, 350–359.
| Water stress enhances expression of an alpha-amylase gene in barley leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xht1Krs7o%3D&md5=e4eb0fcf596c6d06499032c4120e1b3eCAS | 16664625PubMed |
Ji K, Wang Y, Sun W, Lou Q, Mei H, Shen S, Chen H (2012) Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. Journal of Plant Physiology 169, 336–344.
| Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSmsLs%3D&md5=d7e968f7a587125cf2a1a98e1bb985cbCAS | 22137606PubMed |
Jiang Y, Huang B (2001) Physiological responses to heat stress alone or in combination with drought: a comparison between tall fescue and perennial ryegrass. HortScience 36, 682–686.
Jones MGK, Outlaw WH, Lowry OH (1977) Enzymic assay of 10−7 to 10−14 moles of sucrose in plant tissues. Plant Physiology 60, 379–383.
| Enzymic assay of 10−7 to 10−14 moles of sucrose in plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlvVShsbs%3D&md5=767fc32973a053d837d14307e3e05d38CAS |
Jones RJ, Schreiber BMN, Roessler JA (1996) Kernel sink capacity in maize: genotype and maternal regulation. Crop Science 36, 301–306.
| Kernel sink capacity in maize: genotype and maternal regulation.Crossref | GoogleScholarGoogle Scholar |
Kameli A, Losel DM (1995) Contribution of carbohydrates and other solutes to osmotic adjustment in wheat leaves under water stress. Journal of Plant Physiology 145, 363–366.
| Contribution of carbohydrates and other solutes to osmotic adjustment in wheat leaves under water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjs1ars7g%3D&md5=73630449e3ebb162e7b2d4db0a7f1b0cCAS |
Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperature stress. Plant Physiology 126, 120–128.
| Roles of β-amylase and starch breakdown during temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKjuro%3D&md5=4a70433e56a9b483fe7a07667770e00bCAS |
Kashiwagi J, Upadhyaya HD, Krishnamurthy L (2010) Significance and genetic diversity of SPAD chlorophyll meter reading in chickpea germplasm in the semi-arid environments. Journal of Food Legumes 23, 99–105.
Keller F, Ludlow MM (1993) Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan L). Journal of Experimental Botany 44, 1351–1359.
| Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan L).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVGksL4%3D&md5=f3137ee0a732c3a83667d261b93ffe85CAS |
Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310–316.
| Complexity of the heat stress response in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Sit7k%3D&md5=c944b2ea03d522529dda88e85fb83568CAS | 17482504PubMed |
Krishnamurthy L, Kashiwagi J, Gaur PM, Upadhyaya HD, Vadez V (2010) Sources of tolerance to terminal drought in the chickpea (Cicer arietinum L.) minicore germplasm. Field Crops Research 119, 322–330.
| Sources of tolerance to terminal drought in the chickpea (Cicer arietinum L.) minicore germplasm.Crossref | GoogleScholarGoogle Scholar |
Krishnamurthy L, Gaur PM, Basu PS, Chaturvedi SK, Tripathi S, Vadez V, Rathore A, Varshney RK, Gowda CLL (2011) Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm. Plant Genetic Resources; Characterization and Utilization 9, 59–69.
| Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm.Crossref | GoogleScholarGoogle Scholar |
Kumar A, Turner NC (2009) Growth and sucrose synthase activity of developing chickpea (Cicer arietinum L.) seeds under field conditions. Australian Journal of Crop Science 3, 20–27.
Kumar S, Kaushal N, Nayyar H, Gaur P (2012) Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L) seedlings by facilitated accumulation of osmoprotectants. Acta Physiologiae Plantarum 34, 1651–1658.
| Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L) seedlings by facilitated accumulation of osmoprotectants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFeqsL0%3D&md5=ab36f53dbeff8ee1354b5c63309d8fc0CAS |
Larmure A, Salon C, Munier-Jolain NG (2005) How does temperature affect C and N allocation to the seeds during the seed filling period in pea? Effect on seed nitrogen concentration. Functional Plant Biology 32, 1009–1017.
| How does temperature affect C and N allocation to the seeds during the seed filling period in pea? Effect on seed nitrogen concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGmsr%2FO&md5=f7c69ad9c4e346f79c0e6716a7c54d8cCAS |
Leport L, Turner NC, French RJ, Tennant D, Thomson BD, Siddique KHM (1998) Water relations, gas exchange and growth of cool-season grain legumes in a Mediterranean-type environment. European Journal of Agronomy 9, 295–303.
| Water relations, gas exchange and growth of cool-season grain legumes in a Mediterranean-type environment.Crossref | GoogleScholarGoogle Scholar |
Leport L, Turner NC, Davies SL, Siddique KHM (2006) Variation in pod production and abortion among chickpea cultivars under terminal drought. European Journal of Agronomy 24, 236–246.
| Variation in pod production and abortion among chickpea cultivars under terminal drought.Crossref | GoogleScholarGoogle Scholar |
Liu X, Huang B (2000) Carbohydrate accumulation in relation to heat stress tolerance in two creeping bentgrass cultivars. Journal of the American Society for Horticultural Science 125, 442–447.
Liu F, Jensen CR, Andersen MN (2004) Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Research 86, 1–13.
| Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvVGhu78%3D&md5=6656fdc52a022c387f13f3843bdc1a4aCAS |
Liu J, Xie X, Du J, Sun J, Bai X (2008) Effects of simultaneous drought and heat stress on Kentucky bluegrass. Scientia Horticulturae 115, 190–195.
| Effects of simultaneous drought and heat stress on Kentucky bluegrass.Crossref | GoogleScholarGoogle Scholar |
Lo Bianco RL, Rieger M, Sung SS (2003) Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach. Physiologia Plantarum 108, 71–78.
| Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach.Crossref | GoogleScholarGoogle Scholar |
Macar TK, Ekmekci Y (2008) PSII photochemistry and antioxidant responses of a chickpea variety exposed to drought. Zeitschrift fur Naturforschung. C. Journal of Biosciences 63, 583–594.
McCann SE, Huang B (2007) Effects of trinexapac-ethyl foliar application on creeping bentgrass responses to combined drought and heat stress. Crop Science 47, 2121–2128.
| Effects of trinexapac-ethyl foliar application on creeping bentgrass responses to combined drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSltbbP&md5=e5cd00cd2fd5551e37f355a0cb93f614CAS |
McCann SE, Huang BR (2008) Evaluation of drought tolerance and avoidance traits for six creeping bentgrass cultivars. HortScience 43, 519–524.
Mishra KB, Iannacone R, Petrozza A, Mishra A, Armentano N, La Vecchia G, Trtilek M, Cellini F, Nedbal L (2012) Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Science 182, 79–86.
| Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFejurzI&md5=c8d01e07009282ce13d3482fa65e393fCAS | 22118618PubMed |
Müller C, Bondeau A, Popp A, Waha K, Fader M (2009) ‘Climate change impacts on agricultural yields. Background note for the World Development Report 2010.’ (World Bank, Potsdam Institute for Climate Impact Research (PIK): Potsdam, Germany)
Nguyen-Quoc B, Foyer CH (2001) A role for futile cycles involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. Journal of Experimental Botany 52, 881–889.
| A role for futile cycles involving invertase and sucrose synthase in sucrose metabolism of tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVejtb8%3D&md5=e6356c7971c12830b0b9da9b75373e07CAS | 11432905PubMed |
Nygaard P (1977) Utilization of exogenous carbohydrates for tube growth and starch synthesis in pine pollen suspension culture. Physiologia Plantarum 39, 206–210.
| Utilization of exogenous carbohydrates for tube growth and starch synthesis in pine pollen suspension culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhs1yjs7s%3D&md5=674038b9b840ed280a8f8b38b1ad2785CAS |
Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Annals of Botany 89, 833–839.
| Rubisco activity: effects of drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitLo%3D&md5=df12d0dfbda72c6ad92236eb122f4d53CAS |
Premchandra GS, Sameoka H, Ogata S (1990) Cell osmotic membrane stability, an indication of drought tolerance, as affected by applied nitrogen in soil. Journal of Agricultural Research 115, 63–66.
Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress responsive transcriptome anlaysis in heat susceptible and tolerant wheat. BMC Genomics 9, 432–451.
| Heat stress responsive transcriptome anlaysis in heat susceptible and tolerant wheat.Crossref | GoogleScholarGoogle Scholar | 18808683PubMed |
Racker E (1962) Ribulose diphosphate carboxylase from spinach leaves. Methods in Enzymology 5, 266–270.
| Ribulose diphosphate carboxylase from spinach leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFGgu7w%3D&md5=6c50f96e2ce2b4da500b66237359e964CAS |
Ristic Z, Bukovnik U, Prasad PVV (2007) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Science 47, 2067–2073.
| Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSltbbN&md5=7bf91f8ae2474173acb32864c2cef9deCAS |
Rizhsky L, Liang H, Shuman J, Vladimir S, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683–1696.
| When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmsbs%3D&md5=7f93b6e0d04f3773e3aa7cc691a23f9bCAS | 15047901PubMed |
Roitsch T, González MC (2004) Function and regulation of invertases in higher plants: sweet sensations. Trends in Plant Science 9, 607–613.
Rollins JA, Habte E, Templer SE, Colby T, Schmidt J, Von Korff M (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). Journal of Experimental Botany 64, 3201–3212.
| Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CktL%2FF&md5=7a6830af59015160fb28f51b785abdffCAS | 23918963PubMed |
Ruan YL (2012) Signaling role of sucrose metabolism in development. Molecular Plant 5, 763–765.
| Signaling role of sucrose metabolism in development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSlsb7E&md5=1ea6bb8f430f63563d70fe824105fdbaCAS | 22532605PubMed |
Saeedipour S (2011) Activities of sucrose-metabolizing enzymes in grains of two wheat (Triticum aestivum L) cultivars subjected to water stress during grain filling. Journal of Plant Breeding and Crop Science 3, 106–113.
Sainz M, Diaz 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. Plant Physiology 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 | 1:CAS:528:DC%2BC3cXhtFaisrjF&md5=7fa3f92bbebe15307dcedb135cee834fCAS |
Shah NH, Paulsen GM (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant and Soil 257, 219–226.
| Interaction of drought and high temperature on photosynthesis and grain-filling of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Cmurc%3D&md5=03379c6da5122dd7290b061c88551494CAS |
Shuster L, Gifford RH (1962) Changes in 3-nucleaotidases during the germination of wheat embryo. Archieves of Biochemistry and Biophysics 96, 532–540.
Singh DP, Peters DB, Singh P, Singh M (1987) Diurnal patterns of canopy photosynthesis, evapotranspiration and water use efficiency in chickpea (Cicer arietinum L.) under field conditions. Photosynthesis Research 11, 61–69.
| Diurnal patterns of canopy photosynthesis, evapotranspiration and water use efficiency in chickpea (Cicer arietinum L.) under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2czmsVWltQ%3D%3D&md5=0cd2299af42a8d42d8cc2c8e0f7b5199CAS | 24435463PubMed |
Singh RP, Prasad PVV, Sunita K, Giri SN, Reddy KR (2007) Influence of high temperature and breeding for heat tolerance in cotton: a review. Advances in Agronomy 93, 313–385.
| Influence of high temperature and breeding for heat tolerance in cotton: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktlyjsb4%3D&md5=7086381270eca2cedbac88d44b6f6d6eCAS |
Srinivasan A, Takeda H, Senboku T (1996) Heat tolerance in food legumes as evaluated by cell membrane thermostability and chlorophyll fluorescence techniques. Euphytica 88, 35–45.
| Heat tolerance in food legumes as evaluated by cell membrane thermostability and chlorophyll fluorescence techniques.Crossref | GoogleScholarGoogle Scholar |
Steponkus PL, Lanphear FO (1967) Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiology 42, 1423–1426.
| Refinement of the triphenyl tetrazolium chloride method of determining cold injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXpslY%3D&md5=91129d8a51db39a2d60cdd090f382da0CAS | 16656672PubMed |
Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends in Plant Science 4, 401–407.
| The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning.Crossref | GoogleScholarGoogle Scholar | 10498964PubMed |
Sumesh KV, Sharma-Natu P, Ghildiyal MC (2008) Starch synthase activity and heat shock protein in relation to thermal tolerance of developing wheat grains. Plant Biology 52, 749–753.
| Starch synthase activity and heat shock protein in relation to thermal tolerance of developing wheat grains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWiu77P&md5=bf9feafc5652eff21b56daadaa45c2aeCAS |
Summerfield RJ, Hadley P, Roberts EH, Minchin FR, Rawsthorne S (1984) Sensitivities of chickpeas (Cicer arietinum L.) to hot temperatures during the reproductive period. Experimental Agriculture 20, 77–93.
| Sensitivities of chickpeas (Cicer arietinum L.) to hot temperatures during the reproductive period.Crossref | GoogleScholarGoogle Scholar |
Sumner JB, Howell SF (1935) The determination of saccharase. The Journal of Biological Chemistry 108, 51–55.
Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber (Cucumis sativus L.) and wheat (Triticum aestivum L.). Plant Physiology 117, 851–858.
| Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber (Cucumis sativus L.) and wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvVyltro%3D&md5=8f0d52934f7526a1d3ceee83aaa3ada9CAS |
Triboï E, Abad A, Michelena A, Lloveras J, Ollier JL, Daniel C (2000) Environmental effects on the quality of two wheat genotypes: 1. Quantitative and qualitative variation of storage proteins. European Journal of Agronomy 13, 47–64.
| Environmental effects on the quality of two wheat genotypes: 1. Quantitative and qualitative variation of storage proteins.Crossref | GoogleScholarGoogle Scholar |
Triboï E, Martre P, Triboï-Blondel A (2003) Environmentally-induced changes in protein composition in developing grains of wheat are related to changes in total protein content. Journal of Experimental Botany 54, 1731–1742.
| Environmentally-induced changes in protein composition in developing grains of wheat are related to changes in total protein content.Crossref | GoogleScholarGoogle Scholar | 12773520PubMed |
Turner NC, Meyer R (2011) Synthesis of regional impacts and global agricultural adjustments. In ‘Crop adaptation to climate change’. (Eds SS Yadav, RJ Redden, JL Hatfield, H Lotze-Campen, AE Hall) pp. 156–165. (Wiley-Blackwell: Chichester, UK)
Turner NC, Furbank RT, Berger JD, Gremigni P, Abbo S, Leport L (2009) Seed size is associated with sucrose synthase activity in developing cotyledons of chickpea. Crop Science 49, 621–627.
| Seed size is associated with sucrose synthase activity in developing cotyledons of chickpea.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Huang B (2004) Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress. Crop Science 44, 1729–1736.
| Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotVCgurg%3D&md5=e1b5f2f82ee0477dfa3a18f3cb05d8ccCAS |
Wang ZY, Snyder GW, Esau BD, Portis AR, Ogren WL (1992) Species dependent variation in the interaction of substrate‐bound ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiology 100, 1858–1862.
| Species dependent variation in the interaction of substrate‐bound ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFWqtr4%3D&md5=d3360d12c92f9bbbfdd719a9a82bebfbCAS | 16653209PubMed |
Wang J, Gan YT, Clarke F, McDonald CL (2006a) Response of chickpea yield to high temperature stress during reproductive development. Crop Science 46, 2171–2178.
| Response of chickpea yield to high temperature stress during reproductive development.Crossref | GoogleScholarGoogle Scholar |
Wang SJ, Liu LF, Chen CK, Chen LW (2006b) Regulations of granule-bound starch synthase I gene expression in rice leaves by temperature and drought stress. Biologia Plantarum 50, 537–541.
| Regulations of granule-bound starch synthase I gene expression in rice leaves by temperature and drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtlaku7%2FM&md5=bbaae6d5c7c1cce74f729e938bfea5fcCAS |
Wardlaw IF (2002) Interaction between drought and chronic high temperature during kernel filling in wheat in a controlled environment. Annals of Botany 90, 469–476.
| Interaction between drought and chronic high temperature during kernel filling in wheat in a controlled environment.Crossref | GoogleScholarGoogle Scholar | 12324270PubMed |
Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U (2000) Sucrose transport in barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. The Plant Journal 21, 455–467.
| Sucrose transport in barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVeisLc%3D&md5=02f0342ce93d73cd69cb31327442582cCAS | 10758497PubMed |
Wigley TML, Raper SCB (2001) Interpretation of high projections for global-mean warming. Science 293, 451–454.
| Interpretation of high projections for global-mean warming.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvhsVOmsw%3D%3D&md5=b1817a073ea70b3f665301c87a97bbe6CAS |
Wilhelm EP, Mullen RE, Keeling PL, Singletary GW (1999) Heat stress during grain φιlling in maize: effects on kernel growth and metabolism. Crop Science 39, 1733–1741.
| Heat stress during grain φιlling in maize: effects on kernel growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXpt1Grtg%3D%3D&md5=bc3c6243990315209f26c9300fbc33f8CAS |
Xu ZZ, Zhou GS (2006) Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. Planta 224, 1080–1090.
| Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVart7c%3D&md5=4722420dcd07e11432b8c70d5e717db8CAS | 16685524PubMed |
Yadav SS, Kumar J, Yadav SK, Singh S, Yadav VS, Turner NC, Redden R (2006) Evaluation of Helicoverpa and drought resistance in desi and kabuli chickpea. Plant Genetic Resources: Characterization and Utilization 4, 198–203.
| Evaluation of Helicoverpa and drought resistance in desi and kabuli chickpea.Crossref | GoogleScholarGoogle Scholar |
Yang JC, Zhang JH, Wang ZQ, Xu GW, Zhu QS (2004) Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiology 135, 1621–1629.
| Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqs7g%3D&md5=41cf70079570030ed2af0648eebab323CAS |
Yordanov I, Velikova V, Tsonev T (2003) Plant responses to drought and stress tolerance. Bulgarian Journal of Plant Physiology 187–206.
Zinselmeier C, Jeong BR, Boyer JS (1999) Starch and the control of kernel number in maize at low water potentials. Plant Physiology 121, 25–36.
| Starch and the control of kernel number in maize at low water potentials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGls7k%3D&md5=c76bf1b5effbe6f66267d3a1ba374f35CAS | 10482657PubMed |