CURRENT UNDERSTANDING OF THE MECHANISMS OF HEAT STRESS TOLERANCE IN RICE (Oryza sativa L.)

Kananbala  Sarangthem; Seemasundari  Yumlembam; Sheikh  Benazir; Khaling  Mikawlrawng; Rozina  Yendrembam

doi:10.18006/2021.9(Spl-3-NRMCSSA_2021).S321.S329

Authors

Kananbala Sarangthem Manipur University, Canchipur, Department of Botany, Plant Physiology Laboratory, Imphal, Pin code: 795004
Seemasundari Yumlembam Manipur University, Canchipur, Department of Botany, Plant Physiology Laboratory, Imphal, Pin code: 795004
Sheikh Benazir Manipur University, Canchipur, Department of Botany, Plant Physiology Laboratory, Imphal, Pin code: 795004
Khaling Mikawlrawng Manipur University, Canchipur, Department of Botany, Plant Physiology Laboratory, Imphal, Pin code: 795004
Rozina Yendrembam Manipur University, Canchipur, Department of Botany, Plant Physiology Laboratory, Imphal, Pin code: 795004

DOI:

https://doi.org/10.18006/2021.9(Spl-3-NRMCSSA_2021).S321.S329

Keywords:

Rice, Heat stress, Tolerance, Mechanism

Abstract

Various studies reported by scientific communities such as NASA’s Goddard Institute for Space Studies (GISS) indicated an increase in average global temperature by approx. 0.8 °C since 1880. Rice (Oryza sativa L.), a heat sensitive plant cereal crop could be greatly affected by heat stress due to global temperature rise. Thus, it is envisaged that rice productivity could markedly decrease due to a rise in mean atmospheric temperature. Different studies have been reported possible mechanisms of heat stress tolerance in Rice. The present review will therefore discuss the current fundamental understanding of heat tolerant mechanisms involving heat shock proteins, plant hormones, plant growth regulators, osmoprotectants, and the importance of membrane thermal stability in rice.

References

Abdul-Razack M, Lee T (2009) Impact of high night time temperature on respiration, membrane stability, antioxidant capacity, and yield of rice plants. Crop Science 49: 313–322.

Ahmed J, Hasan M (2011) Evaluation of seedling proline content of wheat genotypes in relation to heat tolerance. Bangladesh Journal of Botany 40: 17-22.

Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P ( 2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Frontiers in Plant Science 10 (230): 1-13.

Anwar A, Liu Y, Dong R, Bai L, Yu X, Li Y (2018) The physiological and molecular mechanism of brassinosteroid in response to stress: A review. Biological Research 51 (46): 1-15

Bahuguna RN, Jha J, Pal M, Shah D, Lawas LM, Khetarpal S, Jagadish KSV (2015) Physiological and biochemical characterization of NERICA-L-44: a novel source of heat tolerance at the vegetative and reproductive stages in rice. Physiologia Plantarum 154: 543-559.

Bheemanahalli R, Sathishraj R, Manoharan M, Sumanth HN, Muthurajan R, Ishimaru T, Krishna JSV ( 2017) Is early morning flowering an effective trait to minimize heat stress damage during flowering in rice? Field Crops Research 203: 238–242.

Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Science 21: 43-47.

Chandrakala JU, Chaturvedi AK, Ramesh KV, Rai P, Khetarpal S, Pal M (2013) Acclimation response of signalling molecules for high temperature stress on photosynthetic characteristics in rice genotypes. Indian Journal of Plant Physiology 18: 142–150.

Chang PFL, Jinn TL, Huang WK, Chen Y, Chang HM, Wang CW (2007) Induction of a cDNA clone from rice encoding a class II small heat shock protein by heat stress, mechanical injury, and salicylic acid. Plant Science 172: 64-75.

Das S, Krishnan P, Nayak M, Ramakrishnan B (2014) High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environmental and Experimental Botany 101: 36–46.

De Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. Journal of Plant Physiology 161: 1211-1224.

Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. The Plant Journal 29: 681–691.

Dionisio-Sese ML, Shono M, Tobita S (2000) Effects of proline and betaine on heat inactivation of ribulose-1, 5-bisphosphate carboxylase/oxygenase in crude extracts of rice seedlings. Photosynthetica 36: 557–563.

Fahad S, Ali AB , Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8: 1147.

Fahad S, Hussain S, Saud S, Hassan S, Ihsan Z, Shah AN, Wu C, Yousaf M, Nasim W, Alharby H, Alghabari F, Huang J (2016a) Exogenously applied plant growth regulators enhance the morpho-physiological growth and yield of rice under high temperature. Frontiers in Plant Science 7: 1250.

Fahad S, Hussain S, Saud S, Khan F, Hassan S, Amanullah, Nasim W, Arif M, Wang F, Huang J (2016b) Exogenously applied plant growth regulators affect heat-stressed rice pollens. Journal of Agronomy and Crop Science 202: 139-150.

Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiologiae Plantarum 31(5): 937–945.

Forkar M, Nguyen HT, Blum A (1998) Heat tolerance in spring wheat. I. Estimating cellular thermostability and its heritability. Euphytica 104: 1-8.

Govindaraj M, Pattanashetti SK, Patne N, Kanatti AA (2018) Breeding cultivars for heat stress tolerance in staple food crops. In: Çiftçi YÖ (Ed.) Next generation plant breeding. InTechOpen.

Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: Antioxidant defenses is a key factor. In: Crop Stress and Its Management: Perspectives and Strategies. Springer; Berlin, Germany, 261–316.

Hasanuzzaman M, Nahar K, Fujita M (2013) Extreme temperatures, oxidative stress and antioxidant defense in plants. In: Abiotic Stress: Plant Responses and Applications in Agriculture. InTech; Rijeka, Croatia, Pp. 169–205.

Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: A review. Environmental and Experimental Botany 68: 14–25.

Huang B, Xu C (2008) Identification and characterization of proteins associated with plant tolerance to heat stress. Journal of Integrative Plant Biology 50: 1230-1237.

Jagadish SVK, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany 58: 1627–1635.

Jagadish SVK, Muthurajan R, Oane R, Wheeler T, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice. Journal of Experimental Botany 61: 143–156.

Jain R, Solomon S, Shrivastava AK, Lal P (2001) Nutrient application improves stubble bud sprouting under low temperature conditions in sugarcane. Sugar Tech 11(1):83–85.

Julia C, Dingkuhn M (2012) Variation in time of day of anthesis in rice in different climatic environments. European Journal of Agronomy 43: 166–174.

Julia C, Dingkuhn M (2013) Predicting temperature induced sterility of rice spikelets requires simulation of crop-generated microclimate. European Journal of Agronomy 49: 50–60.

Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Molecular Biology 51: 677-686.

Keller M SPOT-ITN Consortium, Simm S (2018) The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen. BMC Genomics 19: 447.

Kobayasi K, Atsuta Y (2010) Sterility and poor pollination due to early flower opening induced by methyl jasmonate. Plant Production Science 13: 29–36.

Koh S, Lee S Ch, Kim MK, Koh JH, Lee S, An G, Choe S, Kim SR (2007) T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stress. Plant Molecular Biology 65: 453–466.

Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10: 310–316.

Lei G, Zhang HY, Wang ZH, Wei LX, Fu P, Song JB, Fu DH, Huang YJ, Liao JL (2018) High night time temperature induces antioxidant molecule perturbations in heat-sensitive and heat-tolerant coisogenic rice (Oryza sativa) strains. Journal of Agricultural and Food Chemistry 66: 12131–12140.

Levitt J (1980) Responses of plants to environmental stresses. Academic Press, New York.

Maavimani M, Jebaraj S, Raveendran M, Vanniarajan C, Balakrishnan K, Muthamilan M (2014) Cellular membrane thermostability is related to rice (Oryza sativa L) yield under heat stress. International Journal of Tropical Agriculture 32: 201–208.

Maestri E, Klueva N, Perrota C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Molecular Biology 48: 667–681.

Mäkelä P, Karkkainen J, Somersalo S (2000) Effect of glycine betaine on chloroplast ultrastructure, chlorophyll and protein content, and RUBPCO activities in tomato grown under drought or salinity. Biologia Plantarum 3: 471–475.

Mohammed AR, Tarpley L (2011) Effects of night temperature, spikelet position and salicylic acid on yield and yield-related parameters of rice (Oryza sativa L.). Journal of Agronomy and Crop Science 197: 40-49.

Mostofa MG, Yoshida N, Fujita M (2014) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regulation 73(1): 31–44.

Naeem S, Atique-ur-Rehman , Farooq O , Wasaya A , Saliq S , Mubeen K (2019) Improved auxin level at panicle initiation stage enhance the heat stress tolerance in rice plants. In: © Proceedings of the 2019 Agronomy Australia Conference, Australia 1-4.

Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and diferentially modulate antioxidant enzymes and expression of related genes. Journal of Plant Physiology 169(6):596–604.

Oh-e I, Saitoh K, Kuroda T (2007) Effects of high temperature on growth, yield and dry-matter production of rice grown in the paddy field. Plant Production Science 10: 412-422.

Prasad PVV, Bheemanahalli R, Jagadish SVK (2017) Field crops and the fear of heat stress—opportunities, challenges and future directions. Field Crops Research 200: 114–121.

Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnology Journal 2: 477–486.

Rasheed R, Wahid A, Farooq M, Hussain I, Basra SMA (2011) Role of proline and glycine betaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. Plant Growth Regulation 65(1):35–45.

Reynolds MP, Balota M, Delgado MIB, Amani I Fischer RA (1994) Physiological and morphological traits associated with spring wheat yield under hot, irrigated conditions. Australian Journal of Plant Physiology 21: 717-730.

Sadalla MM, Shanahan JF, Quick JS (1990) Heat tolerance in winter wheat. I. Hardening and genetic effects on membrane thermostability. Crop Science 30: 1243-1247.

Sailaja B, Subrahmanyam D, Neelamraju S, Vishnukiran T, Rao YV, Vijayalakshmi P, Voleti SR, Bhadana VP, Mangrauthia SK (2015) Integrated physiological, biochemical, and molecular analysis identifies important traits and mechanisms associated with differential response of rice genotypes to elevated temperature. Frontiers in Plant Science 6: 1044.

Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell and Environment 25(2):163–171.

Satake T, Yoshida S (1978) High temperature induced sterility in indica rices at flowering. Japanese Journal of Crop Science 47: 6–17.

Sheehy JE, Elmido A, Centeno G, Pablico P (2005) Searching for new plants for climate change. Journal of Agricultural Meteorology 60: 463–468.

Sonjaroon W, Thussagunpanit J, Jutamanee K, Khamsuk O, Suksamrarn A (2017) Exposure brassinosteroid and brassinosteroid mimics continually improve photosynthesis in rice subject to heat stress. Agrotechnology 6: 4.

Sullivan CY (1972) Mechanisms of heat and drought resistance in grain sorghum and method of measurements. In: Rao NGP, House LR (Eds.) Sorghum in the seventies Oxford and IBH Publication, New Delhi, 247-264.

Szabados L, Savoure´ A (2010) Proline: A multifunctional amino acid. Trends in Plant Science 15: 89-97.

Tang RS, Zheng JC, Jin ZQ, Zhang DD, Huang YH, Chen LG (2008) Possible correlation between high temperature induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.) Plant Growth Regulation 54:37-43.

Tang S, Zhang H, Li CL, Liu X, Chen L, Chen W, Ding Y (2018) Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period. Functional Plant Biology 45: 911–921.

Tian J, Guo S, Liu X, Zhang R, Cheng Y (2009) Effects of exogenous spermidine pretreatment on antioxidant system in cucumber seedling leaves under high temperature stress. Acta Botanica Boreali Occidentalia Sinica 11: 20.

Wahid A, Gelani S, Ashraf M, Foolad M (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61: 199–223.

Weerakoon WMW, Maruyama A, Ohba K (2008) Impact of humidity on temperature-induced grain sterility in rice (Oryza sativa L.). Journal of Agronomy and Crop Science 194: 135–140.

Xiong D, Yu T, Ling X, Fahad S, Peng S, Li Y, Huang J (2014) Sufficient leaf transpiration and nonstructural carbohydrates are beneficial for high-temperature tolerance in three rice (Oryza sativa) cultivars and two nitrogen treatments. Functional Plant Biology 42: 347–356.

Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proceedings of the National Academy of Sciences 99: 7530–7535.

Yoshida S (1981). Fundamentals of rice crop science. Los Baños, The Philippines: IRRI.

Zeng XC, Zhou, Zhang W, Murofushi N, Kitahara T, Kamuro (1999) Opening of rice floret in rapid response to methyl

jasmonate. Journal of Plant Growth Regulation 18: 153–158.

Zhang CX, Feng BH, Chen TT, Zhang XF,Tao LX, Fu GF (2017) Sugars, antioxidant enzymes and IAA mediate salicylic acid to prevent rice spikelet degeneration caused by heat stress. Journal of Plant Growth Regulation 83: 313–323.

Zhang QL, Wei YX, Peng CL (2018) Effects of endogenous ascorbic acid on resistance to high-temperature stress in excised rice leaves. Photosynthetica 56: 1453–1458.