Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants
Open accessAbstract
High temperature (HT) stress is a major environmental stress that limits plant growth, metabolism, and productivity worldwide. Plant growth and development involve numerous biochemical reactions that are sensitive to temperature. Plant responses to HT vary with the degree and duration of HT and the plant type. HT is now a major concern for crop production and approaches for sustaining high yields of crop plants under HT stress are important agricultural goals. Plants possess a number of adaptive, avoidance, or acclimation mechanisms to cope with HT situations. In addition, major tolerance mechanisms that employ ion transporters, proteins, osmoprotectants, antioxidants, and other factors involved in signaling cascades and transcriptional control are activated to offset stress-induced biochemical and physiological alterations. Plant survival under HT stress depends on the ability to perceive the HT stimulus, generate and transmit the signal, and initiate appropriate physiological and biochemical changes. HT-induced gene expression and metabolite synthesis also substantially improve tolerance. The physiological and biochemical responses to heat stress are active research areas, and the molecular approaches are being adopted for developing HT tolerance in plants. This article reviews the recent findings on responses, adaptation, and tolerance to HT at the cellular, organellar, and whole plant levels and describes various approaches being taken to enhance thermotolerance in plants.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Physiological and biochemical tests, such as analyzing response to gibberellic acid and evaluating pigment synthesis, offer faster alternatives for identifying somaclonal variants.
“Additionally, physiological and biochemical tests offer faster alternatives for identifying somaclonal variants, such as analyzing the plant's response to hormones like gibberellic acid and evaluating pigment synthesis (e.g., chlorophyll and carotenoids [112].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [112]
The Introduction (page unavailable) mentions gibberellic acid as a protectant against heat-stress damage, not as a test for somaclonal variants. Section 7.3 discusses profiling plant responses to temperature stress. Searches for somaclonal variants and gibberellic-acid or pigment-based identification found no passage addressing the claimed faster tests. (LLM, conf=0.74)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Mechanisms of Salinity Tolerance
Munns, R., & Tester, M. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092911 · Cited by 13,792 · see citing works
Oxidative stress and neurodegeneration: where are we now?
Halliwell, B. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03907.x · Cited by 2,614 · see citing works
Abiotic Stress Responses in Plants: Unraveling the Complexity of Genes and Networks to Survive
Sofia, A., de Almeida, A. M., da Silva, A. B., da Silva, J. M., Paula, A., Santos, D., Fevereiro, P., & Sousa Araujo, S. D. (2013) · Abiotic Stress - Plant Responses and Applications in Agriculture · doi:10.5772/52779 · Cited by 106 · see citing works
Flagged first, then by citations
Research works printed but not linked: 129
- [1]Intergovernmental Panel on Climate Change (IPCC) Climate change 2007–The physical science basis Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press Cambridge, UK 2007
- [2]Lobell D.B. Asner G.P. Climate and management contributions to recent trends in U.S. agricultural yields Science 2003 299 10.1126/science.1078475 12586935 · DOI
- [3]Lobell D.B. Field C.B. Global scale climate–Crop yield relationships and the impacts of recent warming Environ. Res. Lett. 2007 2 10.1088/1748-9326/2/1/014002 · DOI · Paper page
- [4]Hasanuzzaman M. Hossain M.A. da Silva J.A.T. Fujita M. Plant Responses and Tolerance to Abiotic Oxidative Stress: Antioxidant Defenses is a Key Factor Crop Stress and Its Management: Perspectives and Strategies Bandi V. Shanker A.K. Shanker C. Mandapaka M. Springer Berlin, Germany 2012 261 316
- [6]Valliyodan B. Nguyen H.T. Understanding regulatory networks and engineering for enhanced drought tolerance in plants Curr. Opin. Plant Biol 2006 9 189 195 16483835
- [8]Janska A. Marsik P. Zelenkova S. Ovesna J. Cold stress and acclimation: What is important for metabolic adjustment? Plant Biol 2010 12 395 405 20522175
- [9]Chinnusamy V. Zhu J. Zhou T. Zhu J.K. Small RNAs: Big Role in Abiotic Stress Tolerance of Plants Advances in Molecular Breeding toward Drought and Salt Tolerant Crops Jenks M.A. Hasegawa P.M. Jain S.M. Springer Dordrecht, The Netherland 2007 223 260
- [10]Shinozaki K. Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance J. Exp. Bot 2007 58 221 227 17075077
- [11]Krasensky J. Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks J. Exp. Bot. 2012 10.1093/jxb/err460 PMC4359903 22291134 · DOI
- [12]Semenov M.A. Halford N.G. Identifying target traits and molecular mechanisms for wheat breeding under a changing climate J. Exp. Bot 2009 60 2791 2804 19487387
- [13]Moreno A.A. Orellana A. The physiological role of the unfolded protein response in plants Biol. Res 2011 44 75 80 21720684
- [16]Hasanuzzaman M. Hossain M.A. Fujita M. Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating the antioxidant defense and methylglyoxal detoxification systems Biol. Trace Elem. Res 2012 149 248 261 22535598
- [18]Hasanuzzaman M. Nahar K. Fujita M. Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages Ecophysiology and Responses of Plants under Salt Stress Ahmad P. Azooz M.M. Prasad M.N.V. Springer New York, NY, USA 2013 25 87
- [19]Hasanuzzaman M. Gill S.S. Fujita M. Physiological role of nitric oxide in plants grown under adverse environmental conditions Plant Acclimation to Environmental Stress Tuteja N. Gill S.S. Springer New York, NY, USA 2013 269 322
- [20]Waraich E.A. Ahmad R. Halim A. Aziz T. Alleviation of temperature stress by nutrient management in crop plants: A review J. Soil Sci. Plant Nutr 2012 12 221 244
- [21]Barnabás B. Jäger K. Fehér A. The effect of drought and heat stress on reproductive processes in cereals Plant Cell Environ 2008 31 11 38 17971069
- [25]Kosová K. Vítámvás P. Prášil I.T. Renaut J. Plant proteome changes under abiotic stress-Contribution of proteomics studies to understanding plant stress response J. Proteom 2011 74 1301 1322 21329772
- [28]Ahuja I. de Vos R.C.H. Bones A.M. Hall R.D. Plant molecular stress responses face climate change Trends Plant Sci 2010 15 664 674 20846898
- [29]Mittler R. Blumwald E. Genetic engineering for modern agriculture: Challenges and perspectives Ann. Rev. Plant Biol 2010 61 443 462 20192746
- [30]Lobell D.B. Schlenker W. Costa-Roberts J. Climate trends and global crop production since 1980 Science 2011 333 616 620 21551030
- [31]McClung C.R. Davis S.J. Ambient thermometers in plants: From physiological outputs towards mechanisms of thermal sensing Curr. Biol 2010 20 1086 1092 21172632
- [33]Suzuki N. Miller G. Morales J. Shulaev V. Torres M.A. Mittler R. Respiratory burst oxidases: The engines of ROS signaling Curr. Opin. Plant Biol 2011 14 691 699 21862390
- [34]Suzuki N. Koussevitzky S. Mittler R. Miller G. ROS and redox signalling in the response of plants to abiotic stress Plant Cell Environ 2012 35 259 270 21486305
- [39]Djanaguiraman M. Prasad P.V.V. Seppanen M. Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system Plant Physiol. Biochem 2010 48 999 1007 20951054
- [41]Suwa R. Hakata H. Hara H. El-Shemy H.A. Adu-Gyamfi J.J. Nguyen N.T. Kanai S. Lightfoot D.A. Mohapatra P.K. Fujita K. High temperature effects on photosynthetic partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes Plant Physiol. Biochem 2010 48 124 130 20106675
- [42]Yin Y. Li S. Liao W. Lu Q. Wen X. Lu C. Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves J. Plant Physiol 2010 167 959 966 20417985
- [44]Tan W. Meng Q.W. Brestic M. Olsovska K. Yang X. Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants J. Plant Physiol 2011 168 2063 2071 21803445
- [52]Toh S. Imamura A. Watanabe A. Okamot M. Jikumaru Y. Hanada A. Aso Y. Ishiyama K. Tamura N. Iuchi S. High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds Plant Physiol 2008 146 1368 1385 18162586 PMC2259091
- [54]Cheng L. Zou Y. Ding S. Zhang J. Yu X. Cao J. Lu G. Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress J. Integr. Plant Biol 2009 51 489 499 19508360
- [57]Wahid A. Physiological implications of metabolites biosynthesis in net assimilation and heat stress tolerance of sugarcane (Saccharum officinarum) sprouts J. Plant Res 2007 120 219 228 17024517
- [58]Srivastava S. Pathak A.D. Gupta P.S. Shrivastava A.K. Srivastava A.K. Hydrogen peroxide-scavenging enzymes impart tolerance to high temperature induced oxidative stress in sugarcane J. Environ. Biol 2012 33 657 661 23029918
- [59]Omae H. Kumar A. Shono M. Adaptation to high temperature and water deficit in the common bean (Phaseolus vulgarisL.) during the reproductive period J. Bot. 2012 10.1155/2012/803413 · DOI
- [60]Koini M.A. Alvey L. Allen T. Tilley C.A. Harberd N.P. Whitelam G.C. Franklin K.A. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4 Curr. Biol 2009 19 408 413 19249207
- [61]Patel D. Franklin K.A. Temperature-regulation of plant architecture Plant Signal. Behav 2009 4 577 579 19820338 PMC2710546
- [64]Yamamoto Y. Aminaka R. Yoshioka M. Khatoon M. Komayama K. Takenaka D. Yamashita A. Nijo N. Inagawa K. Morita N. Quality control of photosystem II: Impact of light and heat stresses Photosynth. Res 2008 98 589 608 18937045
- [65]Crafts-Brandner S.J. Salvucci M.E. Sensitivity of photosynthesis in a C4 plant, maize, to heat stress Plant Physiol 2002 129 1773 1780 12177490 PMC166765
- [66]Yang X. Chen X. Ge Q. Li B. Tong Y. Zhang A. Li Z. Kuang T. Lu C. Tolerance of photosynthesis to photoinhibition, high temperature and drought stress in flag leaves of wheat: A comparison between a hybridization line and its parents grown under field conditions Plant Sci 2006 171 389 397 22980209
- [68]Marchand F.L. Mertens S. Kockelbergh F. Beyens L. Nijs I. Performance of high arctic tundra plants improved during but deteriorated after exposure to a simulated extreme temperature event Glob. Change Biol 2005 11 2078 2089 34991289
- [70]Kumar A. Omae H. Egawa Y. Kashiwaba K. Shono M. Some Physiological Responses of Snap Bean (Phseolus vulgarisL.) to Water Stress during Reproductive Period Proceedings of the International Conference on Sustainable Crop Production in Stress Environment: Management and Genetic Option JNKVV Jabarpur, India 2005 226 227
- [71]Greer D.H. Weedon M.M. Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate Plant Cell Environ 2012 35 1050 1064 22150771
- [75]Young L.W. Wilen R.W. Bonham-Smith P.C. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production J. Exp. Bot 2004 55 485 495 14739270
- [76]Sato S. Kamiyama M. Iwata T. Makita N. Furukawa H. Ikeda H. Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development Ann. Bot 2006 97 731 738 16497700 PMC2803419
- [77]Maheswari M. Yadav S.K. Shanker A.K. Kumar M.A. Venkateswarlu B. Overview of plant stresses: Mechanisms, adaptations and research pursuit Crop Stress and Its Management: Perspectives and Strategies Venkateswarlu B. Shanker A.K. Shanker C. Maheswari M. Springer Dordrecht, The Netherlands 2012 1 18
- [78]Foolad M.R. Breeding for abiotic stress tolerances in tomato Abiotic Stresses: Plant Resistance through Breeding and Molecular Approaches Ashraf M. Harris P.J.C. The Haworth Press Inc New York, NY, USA 2005 613 684
- [82]Tubiello F.N. Soussana J.F. Howden S.M. Crop and pasture response to climate change Proc. Nat. Acad. Sci. USA 2007 104 19686 19690 18077401 PMC2148358
- [89]Hay R.K.M. Porter J.R. The Physiology of Crop Yield Blackwell Publishing Ltd Oxford, UK 2006
- [92]Högy P. Poll C. Marhan S. Kandeler E. Fangmeier A. Impacts of temperature increase and change in precipitation pattern on crop yield and yield quality of barley Food Chem 2013 136 1470 1477 23194550
- [93]Vasseur F. Pantin F. Vile D. Changes in light intensity reveal a major role for carbon balance in Arabidopsis responses to high temperature Plant Cell Environ 2011 34 1563 1576 21707647
- [94]Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions Plant Physiol 2006 141 391 396 16760493 PMC1475469
- [97]Moller I.M. Jensen P.E. Hansson A. Oxidative modifications to cellular components in plants Ann. Rev. Plant Biol 2007 58 459 481 17288534
- [98]Karuppanapandian T. Wang H.W. Prabakaran N. Jeyalakshmi K. Kwon M. Manoharan K. Kim W. 2,4-dichlorophenoxyacetic acid-induced leaf senescence in mung bean (Vigna radiata L. Wilczek) and senescence inhibition by co-treatment with silver nanoparticles Plant Physiol. Biochem 2011 49 168 177 21144762
- [100]Huang B. Xu C. Identification and characterization of proteins associated with plant tolerance to heat stress J. Integr. Plant Biol 2008 50 1230 1237 19017110
- [101]Camejo D. Jiménez A. Alarcón J.J. Torres W. Gómez J.M. Sevilla F. Changes in photosynthetic parameters and antioxidant activities following heat–shock treatment in tomato plants Func. Plant Biol 2006 33 177 187 32689224
- [102]Bavita A. Shashi B. Navtej S.B. Nitric oxide alleviates oxidative damage induced by high temperature stress in wheat Indian J. Exp. Biol 2012 50 372 378 22803328
- [104]Miller G. Schlauch K. Tam R. Cortes D. Torres M.A. Shulaev V. Dangl J.L. Mittler R. The plant NADPH oxidase RbohD mediates rapid, systemic signaling in response to diverse stimuli Sci. Signal. 2009 2 ra45 19690331
- [105]Qi Y. Wang H. Zou Y. Liu C. Liu Y. Wang Y. Zhang W. Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice FEBS Lett 2010 585 231 239 21130768
- [106]Źróbek-Sokolnik A. Temperature stress and responses of plants Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change Ahmad P. Prasad M.N.V. Springer New York, NY, USA 2012 113 134
- [107]Larcher W. Physiological Plant Ecology Springer Berlin, Germany 1995
- [108]Fitter A.H. Hay R.K.M. Environmental Physiology of Plants 3rd ed Academic Press London, UK 2002
- [112]Wang W. Vinocur B. Shoseyov O. Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response Trends Plant Sci 2004 9 244 252 15130550
- [113]Radin J.W. Lu Z. Percy R.G. Zeiger E. Genetic variability for stomatal conductance in Pima cotton and its relation to improvements of heat adaptation Proc. Natl. Acad. Sci. USA 1994 91 7217 7221 11607487 PMC44370
- [114]Queitsch C. Hong S.W. Vierling E. Lindquist S. Hsp101 plays a crucial role in thermotolerance in Arabidopsis Plant Cell 2000 12 479 492 10760238 PMC139847
- [115]Vinocur B. Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations Curr. Opin. Biotechnol 2005 16 123 132 15831376
- [116]Almeselmani M. Deshmukh P.S. Sairam R.K. Kushwaha S.R. Singh T.P. Protective role of antioxidant enzymes under high temperature stress Plant Sci 2006 171 382 388 22980208
- [120]Dat J. Foyer C. Scott I. Change in salicylic acid and antioxidants during induced thermo tolerance in mustard seedlings Plant Physiol 1998 118 1455 1461 9847121 PMC34763
- [121]Apel K. Hirt H. Reactive oxygen species: metabolism, oxidative stress and signal transduction Ann. Rev. Plant Biol 2004 55 373 399 15377225
- [125]Chauhan S. Physiological and Molecular Basis of Heat Tolerance with Emphasis on Oxidative Stress Metabolism in Wheat PhD Thesis HNB Garhwal University Srinagar, Uttaranchal, India 6 2005
- [130]Tuteja N. Integrated calcium signaling in plants Signaling in Plants I Baluska F. Mancuso S. Springer Heidelberg, Germany 2009 29 49
- [132]Ahmad P. Bhardwaj R. Tuteja N. Plant signaling under abiotic stress environment Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change Ahmad P. Prasad M.N.V. Springer New York, NY, USA 2012 297 324
- [134]Proveniers M.C.G. van Zanten M. High temperature acclimation through PIF4 signaling Trends Plant Sci 2013 18 59 64 23040086
- [135]Hasanuzzaman M. Hossain M.A. Fujita M. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings Plant Biotechnol. Rep 2011 5 353 365 21264525
- [136]Hasanuzzaman M. Hossain M.A. Fujita M. Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings Biol. Trace Elem. Res 2011 143 1704 1721 21264525
- [139]Kaushal N. Gupta K. Bhandhari K. Kumar S. Thakur P. Nayyar H. Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism Physiol. Mol. Biol. Plants 2011 17 203 213 23573011 PMC3550571
- [142]Wang L.J. Fan L. Loescher W. Duan W. Liu G.J. Cheng J.S. Luo H.B. Li S.H. Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves BMC Plant Biol 2010 10 34 20178597 PMC2848757
- [143]Chhabra M.L. Dhawan A. Sangwan N. Dhawan K. Singh D. Phtohormones induced amelioration of high temperature stress in Brassica juncea(L.) Proceedings of 16th Australian Research Assembly on Brassicas Ballarat, Australia 10–14 September 2009
- [147]Song L. Ding W. Zhao M. Sun B. Zhang L. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed Plant Sci 2006 171 449 458 25193642
- [150]Cheng L. Sun R. Wang F. Peng Z. Kon F. Spermidine affects the transcriptome responses to high temperature stress in ripening tomato fruit J. Zhejiang Univ. Sci. 2012 283 297 PMC3323944 22467370
- [153]Sakamoto A. Murata N. The role of glycine betaine in the protection of plants from stress: Clues from transgenic plants Plant Cell Environ 2002 25 163 171 11841661
- [160]Hussain S.S. Ali M. Ahmad M. Siddique K.H.M. Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants Biotechnol. Adv 2011 29 300 311 21241790
- [161]Kusano T. Yamaguchi K. Berberich T. Takahashi Y. Advances in polyamine research in 2007 J. Plant Res 2007 120 345 350 17351711
- [164]Konstantinos P.A. Imene T. Panagiotis M.N. Roubelakis-Angelakis K.A. ABA-dependent amine oxidases-derived H2O2 affects stomata conductance Plant Signal. Behav 2010 5 1153 1156 21490422 PMC3115092
- [165]Chang H.C. Tang Y.C. Hayer-Hartl M. Hartl F.U. SnapShot: Molecular chaperones, Part I Cell 2007 128 10.1016/j.cell.2007.01.001 17990378 · DOI
- [166]Baniwal S.K. Bharti K. Chan K.Y. Fauth M. Ganguli A. Kotak S. Mishra S.K. Nover L. Port M. Scharf K.D. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors J. Biosci 2004 29 471 487 15625403
- [167]Prasinos C. Krampis K. Samakovli D. Hatzopoulos P. Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development J. Exp. Bot 2005 56 633 644 15582930
- [168]Swindell W.R. Huebner M. Weber A.P. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways BMC Genom 2007 8 125 PMC1887538 17519032
- [169]Kulz D. Evolution of the cellular stress proteome: From monophyletic origin to ubiquitous function J. Exp. Biol 2003 206 3119 3124 12909693
- [170]Hong S.W. Lee U. Vierling E. Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures Plant Physiol 2003 132 757 767 12805605 PMC167015
- [171]Morrow G. Tanguay R.M. Small heat shock protein expression and functions during development Int. J. Biochem. Cell Biol 2012 44 1613 1621 22502646
- [172]Nover L. Bharti K. Doring P. Mishra S.K. Ganguli A. Scharf K.D. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need Cell Stress Chaper 2001 6 177 189 PMC434399 11599559
- [173]Lee J.H. Hubel A. Schoffl F. Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis Plant J 1995 8 603 612 7496404
- [174]Mishra S.K. Tripp J. Winkelhaus S. Tschiersch B. Theres K. Nover L. Scharf K.D. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato Genes Dev 2002 16 1555 1567 12080093 PMC186353
- [175]Sun W. Bernard C. van de Cotte B. Montagu M.V. Verbruggen N. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression Plant J 2001 27 407 415 11576425
- [176]Wang Y. Ying J. Kuzma M. Chalifoux M. Sample A. McArthur C. Uchacz T. Sarvas C. Wan J. Dennis D.T. Molecular tailoring of farnesylation for plant drought tolerance and yield protection Plant J 2005 43 413 424 16045476
- [177]Miroshnichenko S. Tripp J. Nieden U.Z. Neumann D. Conrad U. Manteuffel R. Immunomodulation of function of small heat shock proteins prevents their assembly into heat stress granules and results in cell death at sub-lethal temperatures Plant J 2005 41 269 281 15634203
- [178]Torok Z. Goloubinoff P. Horvath I. Tsvetkova N.M. Glatz A. Balogh G. Varvasovszki V. Los D.A. Vierling E. Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone mediated refolding Proc. Natl. Acad. Sci. USA 2001 98 3098 3103 11248038 PMC30613
- [179]Reis S.P. Lima A.M. de Souza C.R.B. Recent molecular advances on downstream plant responses to abiotic stress Int. J. Mol Sci 2012 13 8628 8647 22942725 PMC3430256
- [180]Cho E.K. Hong C.B. Over-expression of tobacco NtHSP70–1 contributes to drought-stress tolerance in plants Plant Cell Rep 2006 25 349 358 16365678
- [182]Bohnert H.J. Gong Q. Li P. Ma S. Unraveling abiotic stress tolerance mechanisms—Getting genomics going Curr. Opin. Plant Biol 2006 9 180 188 16458043
- [183]Maestri E. Klueva N. Perrotta C. Gulli M. Nguyen H.T. Marmiroli N. Molecular genetics of heat tolerance and heat shock proteins in cereals Plant Mol. Biol 2002 48 667 681 11999842
- [184]Malik M.K. Slovin J.P. Hwang C.H. Zimmerman J.L. Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance Plant J 1999 20 89 99 10571868
- [185]Liu J. Shono M. Characterization of mitochondria-located small heat shock protein from tomato (Lycopersicon esculentum) Plant Cell Physiol 1999 40 1297 1304 10682350
- [186]Sanmiya K. Suzuki K. Egawa Y. Shono M. Mitochondrial small heat shock protein enhances thermotolerance in tobacco plants FEBS Lett 2004 557 265 268 14741379
- [187]Katiyar-Agarwal S. Agarwal M. Grover A. Heat tolerant basmati rice engineered by over-expression of hsp101 Plant Mol. Biol 2003 51 677 686 12678556
- [188]Lee B.H. Won S.H. Lee H.S. Miyao M. Chung W.I. Kim I.J. Jo J. Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice Gene 2000 245 283 290 10717479
- [190]Ono K. Hibino T. Kohinata T. Suzuki S. Tanaka Y. Nakamura T. Takabe T. Takabe T. Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances the high-temperature tolerance of tobacco during germination and early growth Plant Sci 2001 160 455 461 11166432
- [191]Alia H.H. Sakamoto A. Murata N. Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine Plant J 1998 16 155 161 9839462
- [192]Yang X. Liang Z. Lu C. Genetic engineering of the biosynthesis of glycine betaine enhances photosynthesis against high temperature stress in transgenic tobacco plants Plant Physiol 2005 138 2299 2309 16024688 PMC1183416
- [193]Salvucci M.E. Crafts-Brandner S.J. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis Physiol. Plant 2004 120 179 186 15032851
- [194]Sharkey T.D. Badger M.R. Von-Caemmerer S. Andrews T.J. Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase Photosyn. Res 2001 67 147 156 16228324
- [195]Murakami Y. Tsuyama M. Kobayashi Y. Kodama H. Iba K. Trienoic fatty acids and plant tolerance of high temperature Science 2000 287 476 479 10642547
- [196]Kovtun Y. Chiu W.L. Tena G. Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants Proc. Natl. Acad. Sci. USA 2000 97 2940 2945 10717008 PMC16034
- [197]Rizhsky R. Liang H. Shuman J. Shulaev V. Davletova S. Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress Plant Physiol 2004 134 1683 1696 15047901 PMC419842
- [198]Shi W.M. Muramoto Y. Ueda A. Takabe T. Cloning of peroxisomal ascorbate peroxidase gene from barley and enhanced thermotolerance by overexpressing in Arabidopsis thaliana Gene 2001 273 23 27 11483357
- [199]Davison P.A. Hunter C.N. Horton P. Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis Nature 2002 418 203 206 12110893
- [200]Grover A. Mittal D. Negi M. Lavania D. Generating high temperature tolerant transgenic plants: Achievements and challenges Plant Sci 2013 205–206 38 47 23498861
- [201]Montero-Barrientos M. Hermosa R. Cardoza R.E. Gutiérrez S. Nicolás C. Monte E. Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses J. Plant Physiol 2010 167 659 665 20080316
- [204]Aprile A. Mastrangelo A.M. De Leonardis A.M. Galiba G. Roncaglia E. Ferrari F. De Bellis L. Turchi L. Giuliano G. Cattivelli L. Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome BMC Genom 2009 10 279 PMC2713995 19552804
- [205]Hasanuzzaman M. Nahar K. Fujita M. Ahmad P. Chandna R. Prasad M.N.V. Öztürk M. Enhancing Plant Productivity under Salt Stress—Relevance of Poly-Omics Salt Stress in Plants: Omics, Signaling and Responses Ahmad P. Azooz M.M. Prasad M.N.V. Springer Berlin, Germany 2013 113 156
- [206]Yeh C.H. Kaplinsky N.J. Hu C. Charng Y.Y. Some like it hot, some like it warm: Phenotyping to explore thermotolerance diversity Plant Sci 2012 195 10 23 22920995 PMC3430125
- [207]Wienkoop S. Morgenthal K. Wolschin F. Scholz M. Selbig J. Weckwerth W. Integration of metabolomic and proteomic phenotypes: analysis of data covariance dissects starch and RFO metabolism from low and high temperature compensation response in Arabidopsis thaliana Mol. Cell Proteom 2008 7 1725 1736 PMC2556022 18445580
- [208]Caldana C. Degenkolbe T. Cuadros-Inostroza A. Klie S. Sulpice R. Leisse A. Steinhauser D. Fernie A.R. Willmitzer L. Hannah M.A. High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions Plant J 2011 67 869 884 21575090
- [209]De Block M. Verduyn C. De Brouwer D. Cornelissen M. Poly (ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance Plant J 2005 41 95 106 15610352
- [210]Maruyama K. Takeda M. Kidokoro S. Yamada K. Sakuma Y. Urano K. Fujita M. Yoshiwara K. Matsukura S. Morishita Y. Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A Plant Physiol 2009 150 1972 1980 19502356 PMC2719109
- [211]Hirai M.Y. Klein M. Fujikawa Y. Yano M. Goodenowe D.B. Yamazaki Y. Kanaya S. Nakamura Y. Kitayama M. Suzuki H. Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics J. Biol. Chem 2005 280 25590 25595 15866872
- [212]Deuschle K. Okumoto S. Fehr M. Looger L.L. Kozhukh L. Frommer W.B. Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering Protein Sci 2005 14 2304 2314 16131659 PMC2253473
- [213]Liu H.C. Liao H.Y. Charng Y.Y. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis Plant Cell Environ 2011 34 738 751 21241330
- [214]Rizhsky L. Hongjian L. Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco Plant Physiol 2002 130 1143 1151 12427981 PMC166635
- [215]Penueli L. Liang H. Rozenberg M. Mittler R. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants Plant J 2003 34 187 203 12694594
- [216]Meehl G.A. Stocker T.F. Collins W.D. Friedlingstein P. Gaye A.T. Gregory J.M. Kitoh A. Knutti R. Murphy J.M. Noda A. Global Climate Projections Climate Change 2007 Solomon S. Qin D. Manning M. Chen Z. Marquis M. Averyt K.B. Tignor M. Miller H.L. Cambridge University Press Cambridge, UK 2007 749 845
Cited by
Sorted by citations
Salam, U., Ullah, S., Tang, Z.-H., Elateeq, A. A., Khan, Y., Khan, J., Khan, A., & Ali, S. (2023) · Life · doi:10.3390/life13030706 · Cited by 480 · see citing works
Chopra, R., Burow, G., Burke, J. J., Gladman, N., & Xin, Z. (2017) · BMC Plant Biology · doi:10.1186/s12870-016-0966-2 · Cited by 113 · see citing works
Genetic approaches to enhance multiple stress tolerance in maize
Malenica, N., Dunić, J. A., Vukadinović, L., Cesar, V., & Šimić, D. (2021) · Genes · doi:10.3390/genes12111760 · Cited by 48 · see citing works
Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives
Majumder, S., Igamberdiev, A. U., & Debnath, S. C. (2025) · Agronomy · doi:10.3390/agronomy15061489 · Cited by 46 · see citing works
Saapilin, N. S., Yong, W. T. L., Cheong, B. E., Kamaruzaman, K. A., & Rodrigues, K. F. (2022) · Chemical and Biological Technologies in Agriculture · doi:10.1186/s40538-022-00293-4 · Cited by 18 · see citing works
da Silva Dias, J. C. (2015) · Molecular Approaches to Genetic Diversity · doi:10.5772/60080 · Cited by 13 · see citing works
- Authors
- Hasanuzzaman, M., Nahar, K., Alam, M., Roychowdhury, R., & Fujita, M.
- Affiliations
- Sher-e-Bangla Agricultural University (BD)
- Kagawa University (JP)
- Visva-Bharati University (IN)
- Corresponding author
- Hasanuzzaman, Mirza
- Fujita, Masayuki
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2013-05-03
- Volume
- 14
- Issue
- 5
- Pages
- 9643-9684
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC3676804
- OpenAlex
- W2035556759
- Cited by
- 2,313
- References
- 3
- Citations by year
- 2026: 209 · 2025: 259 · 2024: 263 · 2023: 251 · 2022: 275 · 2021: 260 · 2020: 241 · 2019: 160 · 2018: 124 · 2017: 90 · 2016: 98 · 2015: 55 · 2014: 22 · 2013: 5
- FWCI
- 6.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Chinese Academy of Sciences
- Sher-e-Bangla Agricultural University
- Kunming Institute of Botany, Chinese Academy of Sciences (650201)
- Institute of Botany, Chinese Academy of Sciences
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Effects of Environmental Stressors on Livestock
- Keywords
- heat stress, heat tolerance, heat acclimation, heat avoidance, ion transporters, osmoprotectants, antioxidants, stress signaling, transcriptional regulation, stress tolerance breeding
- MeSH terms
- Acclimatization, Genetic Engineering, Hot Temperature, Heat-Shock Proteins, Plant Proteins, Plants, Stress, Physiological, Oxidative Stress, Plant Physiological Phenomena, Computational Biology, Plants, Genetically Modified, Plant Development
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review