Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants
Abstract
:1. Introduction
2. Plant Response to Heat Stress
2.1. Growth
2.2. Photosynthesis
2.3. Reproductive Development
2.4. Yield
2.5. Oxidative Stress
3. Plant Adaptation to Heat Stress
3.1. Avoidance Mechanisms
3.2. Tolerance Mechanisms
4. Antioxidant Defense in Response to Heat-Induced Oxidative Stress
5. Mechanism of Signal Transduction and Development of Heat Tolerance
6. Use of Exogenous Protectants in Mitigating Heat-Induced Damages
7. Molecular and Biotechnological Strategies for Development of Heat Stress Tolerance in Plants
7.1. Heat-Shock Proteins (HSPs): Master Players for Heat Stress Tolerance
7.2. Genetic Engineering and Transgenic Approaches in Conferring Heat Stress Tolerance in Plants
7.3. Omics Approaches in Developing Heat Stress Tolerance
8. Conclusion and Future Perspective
Acknowledgments
Conflict of Interest
References
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---|---|---|---|---|
Chili pepper (Capsicum annuum) | 38/30 °C (day/night) | Reproductive, maturity and harvesting stage | Reduced fruit width and fruit weight, increased the proportion of abnormal seeds per fruit. | [36] |
Rice (Oryza sativa) | Above 33 °C, 10 days | Heading stage | Reduced the rates of pollen and spikelet fertility. | [37] |
Wheat (Triticum aestivum) | 37/28 °C (day/night), 20 days | Grain filling and maturity stage | Shortened duration of grain filling and maturity, decreases in kernel weight and yield. | [38] |
Wheat (Triticum aestivum) | 30/25 °C day/night | From 60 DAS to maturity stage | Reduced leaf size, shortened period for days to booting, heading, anthesis, and maturity, drastic reduction of number of grains/spike and smaller grain size and reduced yield. | [39] |
Sorghum (Hordeum vulgare) | 40/30 °C (day/night) | 65 DAS to maturity stage | Decreased chlorophyll (chl) content, chl a fluorescence, decreased photosystem II (PSII) photochemistry, Pn and antioxidant enzyme activity and increased ROS content, and thylakoid membrane damage, reduced yield. | [40] |
Rice (Oryza sativa) | 32 °C (night temperature) | Reproductive stage | Decreased yield, increased spikelet sterility, decreased grain length, width and weight. | [41] |
Maize (Zea mays) | 35/27 °C (day/night), 14 days | Reproductive stage | Reduced ear expansion, particularly suppression of cob extensibility by impairing hemicellulose and cellulose synthesis through reduction of photosynthate supply. | [42] |
Rice (Oryza sativa) | 25–42.5 °C | Vegetative growth stage | Decrease in the CO2 assimilation rate. | [43] |
Soybean (Glycine max) | 38/28 °C (day/night), 14 days | Flowering stage | Decreased the leaf Pn and stomatal conductance (gs), increased thicknesses of the palisade and spongy layers, damaged plasma membrane, chloroplast membrane, and thylakoid membranes, distorted mitochondrial membranes, cristae and matrix. | [44] |
Tobacco (Nicotiana tabacum) | 43 °C, 2 h | Early growth stage | Decrease in net photosynthetic rate (Pn), stomatal conductance as well as the apparent quantum yield (AQY) and carboxylation efficiency (CE) of photosynthesis. Reduced the activities of antioxidant enzymes. | [45] |
Okra (Abelmoschus esculentus) | 32 and 34 °C | Throughout the growing period | Reduced yield, damages in pod quality parameters such as fibre content and break down of the Ca-pectate. | [46] |
Maize (Zea mays) | 33–40 °C, 15 days | During Pre-anthesis and silking onwards | Severe effect on plant and ear growth rates. | [47] |
Wheat (Triticum aestivum) | 38 °C, 24 and 48 h | Seedling stage | Decreased chl and relative water content (RWC); diminished antioxidative capacity. | [18] |
Wheat (Triticum aestivum) | 32/24 °C (day/night), 24 h | At the end of spikelet initiation stage | Spikelet sterility, reduced grain yield. | [48] |
Crops | Heat treatments | Protectants | Protective effects | References |
---|---|---|---|---|
Saccharum officinarum | 42 °C, 48 h | 20 mM Pro or GB, 8 h | Restricted the H2O2 generation, improved K+ and Ca2+ contents, and increased the concentrations of free Pro | [138] |
Cicer arietinum | 45/40 °C, 10 days | 10 μM Pro, 10 days | Reduced membrane injury Improved water and chl content Enhanced activities of antioxidants Reduced oxidative stress Enhance activities of enzymes of carbon metabolism | [139] |
Cicer arietinum | 35/30, 40/35 and 45/40 °C as day/night | 10 μM Pro, GB and Tre | Increased growth Less oxidative damages Decreased MDA and H2O2 contents | [140] |
Oryza sativa | 35 °C, 48 h | 0.5 mM SA, 24 h | Decreased electrolyte osmosis Reduced MDA content and O2·− production rate | [141] |
Vitis vinifera | 43 °C, 24 h | 100 μM SA, 24 h | Higher Rubisco activity Increased PSII function Increased photosynthesis | [142] |
Brassica juncea | 47 ± 5 °C | 0.5 & 1 μM ABA, 4 h | Decreased seedling mortality Increased growth | [143] |
Cicer arietinum | 35/30, 40/35 and 45/40 °C as day/night | 2.5 μM ABA | Increased growth Less oxidative damages Decreased MDA and H2O2 contents | [140] |
Phaseolus vulgaris | 34.7 to 35.2 °C | 25, 50 mg L−1 BRs spray | Increased vegetative growth, total yield and quality of pods Increased the total phenolic acids in the pod | [144] |
Brassica juncea | 40 °C, 5 h × 3 days | 1 μM 24-EBL, 8 h | Better growth Increased protein content Enhanced antioxidant defense | [145] |
Brassica juncea | 47 ± 5 °C | 100 μM IAA, 4 h | Decreased seedling mortality Increased growth | [143] |
Brassica juncea | 47 ± 5 °C | 100 μM GA, 4 h | Decreased seedling mortality Increased growth | [143] |
Vitis vinifera | 42 °C, 12 & 18 h | 50 μM JA, 6 h | Upregulation of the activities of antioxidant enzymes | [146] |
Brassica juncea | 47 ± 5 °C | 50 and 100 μM kinetin | Decreased seedling mortality Increased growth | [143] |
Phragmites communis | 45 °C, 2 h | 100 μM SNP and SNAP, 24 h | Decreased H2O2 and MDA contents. Increased activities of SOD, CAT, APX and POD | [147] |
Phaseolus radiatus | 45 °C, 90 min | 150 μM SNP, 60 min | Increased the activities of CAT, SOD and POD | [148] |
Triticum aestivum | 35 ± 2 °C, 4 or 8 h | Arginine or Put (0.0, 1.25 and 2.5 mM), 4 or 8 h | Increased SOD and CAT activities, increased DNA and RNA contents, reduced MDA level | [149] |
Solanum lycopersicum | 33/27 °C, 16/8 h (light/dark) | Spd, 1 mM as pretreatment | Increase in the expression of Eth-related genes, PA biosynthesis genes, hormone pathways genes, and oxidation reduction genes | [150] |
Gossypium hirsutum | 38 °C up to flowering stage | 10 mM Put, 24 h prior to anthesis | Increased endogenous Put content and seeds/cotton boll | [151] |
Triticum aestivum | 45 °C in germinated seeds, 2 h | Put, 10 μM | Elevated activities of enzymatic and non-enzymatic antioxidants and DAO and PAO, reduced lipid peroxides in root and shoot | [152] |
Sorghum bicolor | 40/30 °C, 45 days | 75 mg L−1 Na2SeO4 foliar spray | Decreased membrane damage Enhanced antioxidant defense Increased grain yield | [40] |
Major classes of heat shock protein | Functions |
---|---|
HSP100 | ATP-dependent dissociation and degradation of aggregate protein |
HSP90 | Co-regulator of heat stress linked signal transduction complexes and manages protein folding. It requires ATP for its function |
HSP70, HSP40 | Primary stabilization of newly formed proteins, ATP-dependent binding and release |
HSP60, HSP10 | ATP-dependent specialized folding machinery |
HSP20 or small HSP (sHSP) | Formation of high molecular weight oligomeric complexes which serve as cellular matrix for stabilization of unfolded proteins. HSP100, HSP70 and HSP40 are needed for its release |
Transgenic plants | Transgenes | Function of transgenes | References |
---|---|---|---|
Z. mays and O. sativa | Hsp100, Hsp101 from A. thaliana | HSP synthesis for HT tolerance | [114,187] |
A. thaliana | Hsp70 | HSP synthesis for thermotolerance | [201] |
N. tabacum | Fad 7 from N. tabacum and O. sativa | Desaturation of fatty acids (trienoic fatty acids and hexa-decatrienoic acid) that increased the level of unsaturated fatty acids and provide HT tolerance | [195,202] |
Daucus carota | Hsp17.7 from D. carota | Synthesis of sHsp | [184,189] |
N. tabacum | TLHS1 | Synthesis of sHSP (Class I) | [203] |
A. thaliana | AtHSF1 | Heat shock transcription factor HSF1::GUS (β-glucuronidase) fusion and such modification will increase HSP production in large scale with small investment of HSFs | [173] |
A. thaliana | gusA | β-glucuronidase synthesis and bind with HSFs to form active trimer | [173] |
N. tabacum | MT-sHSP from L. esculentum | Molecular chaperone function in vitro | [185,186] |
N. tabacum | Dnak1 from Aphanothece halophytica | High temperature tolerance | [190] |
N. tabacum | BADH (betain aldehyde dehydrogenase) from Spinacia oleracea | Over production of GB osmolyte that will enhance the heat tolerance | [192] |
A. thaliana | Cod A (choline oxidase A) from A. globiformis | Glycine betaine systhesis for tolerance to HT during imbibition and seedling germination | [191] |
N. tabacum | ANP1/NPK1 | H2O2 responsive MAPK kinase kinase (MAPKKK) production to protect against the lethality in HT | [196] |
A. thaliana | Ascorbate peroxidase (APX1 from P. sativum and HvAPX1 from H. vulgare) | H2O2 detoxification and conferred heat tolerance | [198] |
© 2013 by the authors; licensee MDPI, Basel, Switzerland This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
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Hasanuzzaman, M.; Nahar, K.; Alam, M.M.; Roychowdhury, R.; Fujita, M. Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants. Int. J. Mol. Sci. 2013, 14, 9643-9684. https://doi.org/10.3390/ijms14059643
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M. Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants. International Journal of Molecular Sciences. 2013; 14(5):9643-9684. https://doi.org/10.3390/ijms14059643
Chicago/Turabian StyleHasanuzzaman, Mirza, Kamrun Nahar, Md. Mahabub Alam, Rajib Roychowdhury, and Masayuki Fujita. 2013. "Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants" International Journal of Molecular Sciences 14, no. 5: 9643-9684. https://doi.org/10.3390/ijms14059643