Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Effects of individual and combined heat and drought stress during seed filling on the oxidative metabolism and yield of chickpea (Cicer arietinum) genotypes differing in heat and drought tolerance

Rashmi Awasthi A , Pooran Gaur B , Neil C. Turner C , Vincent Vadez B , Kadambot H. M. Siddique C and Harsh Nayyar A D
+ Author Affiliations
- Author Affiliations

A Department of Botany, Panjab University, Chandigarh 160014, India.

B ICRISAT, Patancheru 502 324, Greater Hyderabad, Telengana, India.

C The UWA Institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, M082, Locked Bag 5005, Perth, WA 6001, Australia.

D Corresponding author. Email: harshnayyar@hotmail.com

Crop and Pasture Science 68(9) 823-841 https://doi.org/10.1071/CP17028
Submitted: 18 January 2017  Accepted: 6 September 2017   Published: 18 October 2017

Abstract

Drought and heat stress are two major constraints that limit chickpea (Cicer arietinum L.) yield, particularly during seed filling. The present study aimed (i) to assess the individual and combined effects of drought and heat stress on oxidative metabolism during seed filling, and (ii) to determine any genetic variation in oxidative metabolism among genotypes differing in drought and heat tolerance and sensitivity. The plants were raised in outdoor conditions with two different times of sowing, one in November (normal-sown, temperatures <32°C−20°C (day–night) during seed filling), and the other in February (late-sown, temperatures >32°C−20°C (day–night) during seed filling). Plants were regularly irrigated to prevent any water shortage until the water treatments were applied. At both sowing times, the drought treatment was applied during seed filling (at ~75% podding) by withholding water from half of the pots until the relative leaf water content (RLWC) of leaves on the top three branches reached 42–45%, whereas leaves in the fully irrigated control plants were maintained at RLWC 85–90%. Drought-stressed plants were then rewatered and maintained under fully irrigated conditions until maturity. Several biochemical parameters were measured on the leaves and seeds at the end of the stress treatments, and seed yield and aboveground biomass were measured at maturity. Individual and combined stresses damaged membranes, and decreased PSII function and leaf chlorophyll content, more so under the combined stress treatment. The levels of oxidative molecules (malondialdehyde (MDA) and H2O2) markedly increased compared with the control plants in all stress treatments, especially across genotypes in the combined heat + drought stress treatment (increases in leaves: MDA 5.4–8.4-fold and H2O2 5.1–7.1-fold; in seeds: MDA 1.9–3.3-fold and H2O2 3.8–7.9-fold). The enzymatic and non-enzymatic antioxidants related to oxidative metabolism increased under individual stress treatments but decreased in the combined heat + drought stress treatment. Leaves had higher oxidative damage than seeds, and this likely inhibited their photosynthetic efficiency. Yields were reduced more by drought stress than by heat stress, with the lowest yields in the combined heat + drought stress treatment. Heat- and drought-tolerant genotypes suffered less damage and had higher yields than the heat- and drought-sensitive genotypes under the individual and combined stress treatments, suggesting partial cross-tolerance in these genotypes. A drought-tolerant genotype ICC8950 produced more seed yield under the combined heat + drought stress than other genotypes, and this was associated with low oxidative damage in leaves and seeds.

Additional keywords: ascorbate peroxidase, catalase, chlorophyll content, electrolyte leakage, glutathione reductase, superoxide dismutase.


References

Akitha Devi MK, Giridhar DP (2015) Variations in physiological response, lipid peroxidation, antioxidant enzyme activities, proline and isoflavones content in soybean varieties subjected to drought stress. Proceedings of the National Academy of Sciences. India. Section B, Biological Sciences 85, 35–44.
Variations in physiological response, lipid peroxidation, antioxidant enzyme activities, proline and isoflavones content in soybean varieties subjected to drought stress.CrossRef | 1:CAS:528:DC%2BC2MXmsV2quro%3D&md5=55a19fa4ff90988c1eb60f648710e708CAS |

Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Science 171, 382–388.
Protective role of antioxidant enzymes under high temperature stress.CrossRef | 1:CAS:528:DC%2BD28Xmslyksrc%3D&md5=8d9a7dc3df60d9223b04975257806e24CAS |

Almeselmani M, Deshmukh PS, Chinnusamy V (2012) Effect of prolonged high temperature stress on respiration, photosynthesis and gene expression in wheat (Triticum aestivum L.) varieties differing in their thermotolerance. Plant Stress 6, 25–32.

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.CrossRef | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=c59edc954fcfb7562d44253a2051f700CAS |

Ara N, Nakkanong K, Zhang M (2013) Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two cucurbit species (“Cucurbita maxima” and “Cucurbita moschata”) and their interspecific inbred line “Maxchata”. International Journal of Molecular Sciences 14, 24008–24028.
Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two cucurbit species (“Cucurbita maxima” and “Cucurbita moschata”) and their interspecific inbred line “Maxchata”.CrossRef |

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 | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=eda4b05cce26c669ba5e8cab689eb0a4CAS |

Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.CrossRef | 1:CAS:528:DyaK1MXkt1yktr0%3D&md5=50ec896733b7b8582d827531f94d5abfCAS |

Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KHM, Nayyar H (2014) Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Functional Plant Biology 41, 1148–1167.
Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea.CrossRef | 1:CAS:528:DC%2BC2cXhs1ymt7vP&md5=834fb693077098767a8e286d99e6f5adCAS |

Bahar B, Yildirim M (2010) Heat and drought resistances criteria in spring bread wheat: drought resistance parameters. Scientific Research and Essays 5, 1742–1745.

Barnabas 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.

Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. The Journal of Biological Chemistry 272, 20313–20316.
Protein oxidation in aging, disease, and oxidative stress.CrossRef | 1:CAS:528:DyaK2sXlsFKhsbw%3D&md5=32046b02d2727d5c169b3392db48fdd5CAS |

Bhattacharjee S (2012) The language of reactive oxygen species signalling in plants. Le Journal de Botanique 22, 985298

Boaretto LS, Carvalho G, Borgo L, Creste S, Landell MGA, Mazzafera P, Azevedo RA (2014) Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes. Plant Physiology and Biochemistry 74, 165–175.
Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes.CrossRef | 1:CAS:528:DC%2BC2cXhtF2mtrk%3D&md5=8677a7e1004b8283486bdf082422c28cCAS |

Canci H, Toker C (2009) Evaluation of yield criteria for drought and heat resistance in chickpea (Cicer arietinum L.). Journal of Agronomy & Crop Science 195, 47–54.
Evaluation of yield criteria for drought and heat resistance in chickpea (Cicer arietinum L.).CrossRef |

Chakraborty U, Pradhan D (2011) High temperature-induced oxidative stress in Lens culinaris, role of antioxidants and amelioration of stress by chemical pre-treatments. Journal of Plant Interactions 6, 43–52.
High temperature-induced oxidative stress in Lens culinaris, role of antioxidants and amelioration of stress by chemical pre-treatments.CrossRef |

Chugh V, Kumar N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian Journal of Biochemistry & Biophysics 48, 47–53.

Chugh V, Kaur N, Grewal MS, Gupta AK (2013) Differential antioxidative response of tolerant and sensitive maize (Zea mays L.) genotypes to drought stress at reproductive stage. Indian Journal of Biochemistry & Biophysics 50, 150–158.

D’Souza MR, Devaraj VR (2011) Specific and non-specific responses of hyacinth bean (Dolichos lablab) to drought stress. Indian Journal of Biotechnology 10, 130–139.

Davies SL, Turner NC, Siddique KHM, Plummer JA, Leport L (1999) Seed growth of desi and kabuli chickpea (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 (Cicer arietinum L.) in a short-season Mediterranean-type environment.CrossRef |

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 |

Devi R, Narinder K, Anil KG (2012) Potential of antioxidant enzymes in depicting drought tolerance of wheat (Triticum aestivum L.). Indian Journal of Biochemistry & Biophysics 49, 257–265.

Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased level of membrane permeability and lipid peroxidation and decreased level of superoxide dismutase and catalase. Journal of Experimental Botany 32, 93–101.
Leaf senescence: correlated with increased level of membrane permeability and lipid peroxidation and decreased level of superoxide dismutase and catalase.CrossRef | 1:CAS:528:DyaL3MXkt1Wgur0%3D&md5=0f11f200672a0319095780a8c8edbb80CAS |

Du Y-L, Wang Z-Y, Fan J-W, Turner NC, Wang T, Li F-M (2012) β-aminobutyric acid increases abscisic acid accumulation, and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying. Journal of Experimental Botany 63, 4849–4860.
β-aminobutyric acid increases abscisic acid accumulation, and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying.CrossRef | 1:CAS:528:DC%2BC38Xht1KjsLfF&md5=ccd63212a58f949484940518f65d1ce8CAS |

Du Y-L, Wang Z-Y, Fan J-W, Turner NC, He J, Wang T, Li F-M (2013) Exogenous abscisic acid reduces water loss and improves antioxidant defense, desiccation tolerance and transpiration efficiency in two spring wheat cultivars subjected to a soil water deficit. Functional Plant Biology 40, 494–506.
Exogenous abscisic acid reduces water loss and improves antioxidant defense, desiccation tolerance and transpiration efficiency in two spring wheat cultivars subjected to a soil water deficit.CrossRef | 1:CAS:528:DC%2BC3sXnsFSnsrY%3D&md5=bf553a0a32f43a92a1014b5a6ce50e17CAS |

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29, 185–212.
Plant drought stress: effects, mechanisms and management.CrossRef |

Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2016) Drought stress in grain legumes during reproduction and grain filling. Journal of Agronomy & Crop Science 203, 81–102.
Drought stress in grain legumes during reproduction and grain filling.CrossRef |

Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355–364.
Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria.CrossRef | 1:CAS:528:DC%2BD3sXoslekt74%3D&md5=2a794a67bb9d7eb329b92c9fcea3bdb8CAS |

Gan Y, Wang J, Angadi SV, Mcdonald CL (2004) Response of chickpea to short periods of high temperature and water stress at different developmental stages. In ‘Proceedings 4th International Crop Science Congress’. 26 September–1 October 2004, Brisbane, Qld. (International Crop Science Society)

Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.CrossRef | 1:CAS:528:DC%2BC3cXhtlKnu7fF&md5=0bb4cf46349b224aab5e3b008ba65f73CAS |

Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106, 207–212.
Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine.CrossRef | 1:CAS:528:DyaL3cXlt1ygs7k%3D&md5=365e58e121f7968dfd32aed534ec779aCAS |

Grigorova B, Vassileva V, Klimchuk D, Vaseva I, Demirevska K, Feller U (2012) Drought, high temperature, and their combination affect ultrastructure of chloroplasts and mitochondria in wheat (Triticum aestivum L.) leaves. Journal of Plant Interactions 7, 204–213.
Drought, high temperature, and their combination affect ultrastructure of chloroplasts and mitochondria in wheat (Triticum aestivum L.) leaves.CrossRef |

Hall AE (2004) Breeding for adaptation to drought and heat in cowpea. European Journal of Agronomy 21, 447–454.
Breeding for adaptation to drought and heat in cowpea.CrossRef |

Hamidou F, Halilou O, Vadez V (2013) Assessment of groundnut under combined heat and drought stress. Journal of Agronomy & Crop Science 199, 1–11.
Assessment of groundnut under combined heat and drought stress.CrossRef |

Harb A, Awad D, Samarah N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought. Journal of Plant Interactions 10, 109–116.
Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought.CrossRef | 1:CAS:528:DC%2BC2MXovVOrsrk%3D&md5=417881e596e5794c0668f584822851ebCAS |

Hasanuzzaman M, Hossain MA, da Silva T, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defenses are key factors. In ‘Crop stress and its management: perspectives and strategies’. (Eds V Bandi, AK Shanker, C Shanker, M Mandapaka) pp. 261–316. (Springer: Berlin)

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts-I: Kinetics stoichiometry of fatty peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts-I: Kinetics stoichiometry of fatty peroxidation.CrossRef | 1:CAS:528:DyaF1cXhtFWgtLw%3D&md5=5a64786b0ab4716b52c7ba52084fde2dCAS |

Jin R, Wang Y, Liu R, Gou J, Chan Z (2015) Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Frontiers in Plant Science 6, 1123

Karataş I, Ozturk L, Demir Y, Unlukara A, Kurunc A, Duzdemir O (2014) Alterations in antioxidant enzyme activities and proline content in pea leaves under long-term drought stress. Toxicology and Industrial Health 30, 693–700.
Alterations in antioxidant enzyme activities and proline content in pea leaves under long-term drought stress.CrossRef |

Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiology and Molecular Biology of Plants 17, 203–213.
Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism.CrossRef | 1:CAS:528:DC%2BC3MXht1Kjs7nN&md5=807884499b3c26fc2c21b26aca076eb0CAS |

Kebede H, Fisher DK, Young LD (2012) Determination of moisture deficit and heat stress tolerance in corn using physiological measurements and a low-cost microcontroller-based monitoring system. Journal of Agronomy & Crop Science 198, 118–129.
Determination of moisture deficit and heat stress tolerance in corn using physiological measurements and a low-cost microcontroller-based monitoring system.CrossRef |

Khanna-Chopra R, Selote DS (2007) Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than -susceptible wheat cultivar under field conditions. Environmental and Experimental Botany 60, 276–283.
Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than -susceptible wheat cultivar under field conditions.CrossRef | 1:CAS:528:DC%2BD2sXislWgtLg%3D&md5=42ee865248ec643d55be7d7e3a25ed53CAS |

Kolupaev YY, Yastreb TO, Karpets YV, Miroshnichenko NN (2011) Influence of salicylic and succinic acid on antioxidant enzymes activity, heat resistance and productivity of Panicum miliaceum L. Journal of Stress Physiology and Biochemistry 7, 154–163.

Kopczewski T, Kuzniak E (2013) Redox signals as a language of interorganellar communication in plant cells. Central European Journal of Biology 8, 1153–1163.

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 |

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 9, 59–69.
Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm.CrossRef |

Kumar S, Kaur R, Kaur N, Bhandhari K, Kaushal N, Gupta K, Bains TS, Nayyar H (2011) Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiologiae Plantarum 33, 2091–2101.
Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress.CrossRef | 1:CAS:528:DC%2BC38XksleitQ%3D%3D&md5=41e2fa6eb1c28690c631d5f686ea6dd0CAS |

Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiologiae Plantarum 34, 75–86.
Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants.CrossRef | 1:CAS:528:DC%2BC38Xkt1eqsrs%3D&md5=ee9200c3784398ea284d7f7c30d3c853CAS |

Kumar RR, Sharma SK, Goswami S, Singh GP, Singh R, Singh K, Pathak H, Rai RD (2013a) Characterization of differentially expressed stress-associated proteins in starch granule development under heat stress in wheat (Triticum aestivum L.). Indian Journal of Biochemistry & Biophysics 50, 126–138.

Kumar S, Thakur P, Kaushal N, Malik JA, Gaur P, Nayyar H (2013b) Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity. Archives of Agronomy and Soil Science 59, 823–843.
Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity.CrossRef | 1:CAS:528:DC%2BC38XmtFersro%3D&md5=c7b2145d11343a3aeaf13908113ce3c8CAS |

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 |

Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. International Agrophysics 27, 463–477.
Effect of drought and heat stresses on plant growth and yield: a review.CrossRef |

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–275.

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 | 1:CAS:528:DC%2BD3MXlvFShtbo%3D&md5=8176e17c99fb1e8a7f352befd7a362cbCAS |

Mansoor S, Naqvi FN (2013) Effect of heat stress on lipid peroxidation and antioxidant enzymes in mungbean (Vigna radiata L.) seedlings. African Journal of Biotechnology 12, 3196–3203.

Mavis RD, Stellwagen E (1968) Purification and subunit structure of glutathione reductase from bakers’ yeast. The Journal of Biological Chemistry 243, 809–814.

Mishra KB, Iannacone R, Petrozza A, Mishra A, Armentano N, LaVecchia 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 | 1:CAS:528:DC%2BC3MXhsFejurzI&md5=3740d16367e234159af2dcda99e2f52bCAS |

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Oxidative stress, antioxidants and stress tolerance.CrossRef | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=72b5d65ff5dfaea8b5f46673e84bceb8CAS |

Mohammed AR, Tarpley L (2010) Effects of high night temperature and spikelet position on yield-related parameters of rice (Oryza sativa L.) plants. European Journal of Agronomy 33, 117–123.
Effects of high night temperature and spikelet position on yield-related parameters of rice (Oryza sativa L.) plants.CrossRef |

Mukherjee SP, Chaudhari MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Plant Physiology 58, 166–170.
Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings.CrossRef | 1:CAS:528:DyaL3sXksFSgt7g%3D&md5=dcc6f138188931829b53434d72b8b419CAS |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.

Nayyar H, Gupta D (2006) Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. Environmental and Experimental Botany 58, 106–113.
Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants.CrossRef | 1:CAS:528:DC%2BD28Xosl2kt74%3D&md5=b8cc760f0e217b5f5c48ffe17f426af1CAS |

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Ascorbate and glutathione: keeping active oxygen under control.CrossRef | 1:CAS:528:DyaK1cXjvVShtrc%3D&md5=af7dd1b169dcefe9f803fbd497850967CAS |

Osman HS (2015) Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Annals of Agricultural Science 60, 389–402.
Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline.CrossRef |

Pandey V, Shukla A (2015) Acclimation and tolerance strategies of rice under drought stress. Rice Science 22, 147–161.
Acclimation and tolerance strategies of rice under drought stress.CrossRef |

Patel PK, Hemantaranjan A (2012) Salicylic acid induced alteration in dry matter partitioning, antioxidant defense system and yield in chickpea (Cicer arietinum) under drought stress. Asian Journal of Crop Science 4, 86–102.
Salicylic acid induced alteration in dry matter partitioning, antioxidant defense system and yield in chickpea (Cicer arietinum) under drought stress.CrossRef |

Patel PK, Hemantaranjan A, Sarma BK, Singh R (2011) Growth and antioxidant system under drought stress in chickpea (Cicer arietinum L.) as sustained by salicylic acid. Journal of Stress Physiology and Biochemistry 7, 130–144.

Prasad PVV, Staggenborg SA, Ristic Z (2008) Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. In ‘Response of crops to limited water: understanding and modeling water stress effects on plant growth processes’. (Eds LH Ahuja, SA Saseendran) pp. 301–355. (ASA, CSSA: Madison, WI, USA)

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.

Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant Cell 12, 479–492.
Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD3cXktFWisr4%3D&md5=fd3841c1ad03cbd9203323ed5dfb8efeCAS |

Rai N, Rai KK, Tiwari G, Singh PK (2015) Changes in free radical generation, metabolites and antioxidant defense machinery in hyacinth bean (Lablab purpureus. L) in response to high temperature stress. Acta Physiologiae Plantarum 37, 46
Changes in free radical generation, metabolites and antioxidant defense machinery in hyacinth bean (Lablab purpureus. L) in response to high temperature stress.CrossRef |

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 | 1:CAS:528:DC%2BC3sXht1CktL%2FF&md5=3718fa97971c2239a4925f9a79cc03ddCAS |

Saed-Moucheshi A, Shekoofa A, Pessarakli M (2014) Reactive oxygen species (ROS) generation and detoxifying in plants. Journal of Plant Nutrition 37, 1573–1585.
Reactive oxygen species (ROS) generation and detoxifying in plants.CrossRef | 1:CAS:528:DC%2BC2cXmvFKg&md5=7f6a83875ae275cde9746bdad15a01bfCAS |

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. 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 | 1:CAS:528:DC%2BC3cXhtFaisrjF&md5=e8239d24c7396c7b9a78fcb8cb9b402fCAS |

Sairam RK, Srivastava GC, Saxena DC (2000) Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. Biologia Plantarum 43, 245–251.
Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes.CrossRef | 1:CAS:528:DC%2BD3cXksFSitL8%3D&md5=29b95bdf6663eba737e48edb7ee1a713CAS |

Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum 49, 85–91.
Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes.CrossRef | 1:CAS:528:DC%2BD2MXlslKhs78%3D&md5=0987e3042327d8cd0dac884633229447CAS |

Saleh AAH, Abdel-Kader DZ, El-Elish AM (2007) Role of heat shock and salicylic acid in antioxidant homeostasis in mungbean (Vigna radiata L.) plants subjected to heat stress. American Journal of Plant Physiology 2, 344–355.
Role of heat shock and salicylic acid in antioxidant homeostasis in mungbean (Vigna radiata L.) plants subjected to heat stress.CrossRef | 1:CAS:528:DC%2BD1cXjtlykuro%3D&md5=0b78ae4abd1600d09a0a56740f884cbeCAS |

Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environmental and Experimental Botany 99, 141–149.
Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress.CrossRef | 1:CAS:528:DC%2BC2cXislOiu7k%3D&md5=15427db89246989c0af0d871d8b27c1bCAS |

Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage and antioxidative defence mechanisms in plants under stressful conditions. Le Journal de Botanique 2012, 217037

Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologia Plantarum 126, 45–51.
Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction.CrossRef | 1:CAS:528:DC%2BD28XisFKjtbg%3D&md5=9756c7760819a420bcb0e97fc204b554CAS |

Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment 35, 259–270.
ROS and redox signalling in the response of plants to abiotic stress.CrossRef | 1:CAS:528:DC%2BC38XjtVKnsL0%3D&md5=18104f9a9412f507074f64fbc5bc6703CAS |

Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytologist 203, 32–43.
Abiotic and biotic stress combinations.CrossRef |

Tan W, Meng QW, Brestic M, Olsovska K, Yang X (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. Journal of Plant Physiology 168, 2063–2071.
Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants.CrossRef | 1:CAS:528:DC%2BC3MXht12rt73P&md5=4a9acc6da765e63cd3e9c10eadcd8163CAS |

Teranishi Y, Tanaka A, Osumi M, Fukui S (1974) Catalase activity of hydrocarbon utilizing Candida yeast. Agricultural and Biological Chemistry 38, 1213–1220.
Catalase activity of hydrocarbon utilizing Candida yeast.CrossRef | 1:CAS:528:DyaE2cXlsVyitLY%3D&md5=83bcc11f126ec70e907e1a1ef798f662CAS |

Tuteja N, Tiburcio AF, Gill SS, Tuteja R (2012) ‘Improving crop resistance to abiotic stress.’ (Wiley-VCH: Weinheim, Germany)

Voothuluru P, Sharp RE (2013) Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. Journal of Experimental Botany 64, 1223–1233.
Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance.CrossRef | 1:CAS:528:DC%2BC3sXktFKru74%3D&md5=b3119fb42cc1899d88919165e6fc8247CAS |

Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. Journal of Experimental Botany 53, 1227–1236.
Signal transduction during oxidative stress.CrossRef | 1:CAS:528:DC%2BD38XktFSls7w%3D&md5=043192ab69b236a8aec05c2e38c62e86CAS |

Wang X, Dinler BS, Vignjevic M, Jacobsenc S, Wollenweber B (2015) Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars. Plant Science 230, 33–50.
Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars.CrossRef | 1:CAS:528:DC%2BC2cXhvV2gs77K&md5=9995bcad32f6a17c0fcf69da9b115892CAS |

Wang JY, Turner NC, Liu YX, Siddique KHM, Xiong YC (2016) Effects of drought stress on morphological, physiological and biochemical characteristics of wheat species differing in ploidy level. Functional Plant Biology 44, 219–234.
Effects of drought stress on morphological, physiological and biochemical characteristics of wheat species differing in ploidy level.CrossRef |



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