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Heat Shock Proteins in Plant Protection from Oxidative Stress

  • OXIDATIVE STRESS AND ANTIOXIDANT DEFENSE SYSTEMS
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Abstract—This review considers the recent progress on the role of heat shock proteins (HSPs), as well as transcription factors of heat shock proteins genes (HSFs) in protecting plants from oxidative stress induced by various types of abiotic and biotic stresses. HSPs are pleiotropic proteins involved in various intracellular processes and performing many important functions. In particular, HSPs increase plant resistance to stress by protecting the structure and activity of proteins of the antioxidant system. Overexpression of Hsp genes under stressful conditions, leading to an increased content of HSPs, can be used as a marker of oxidative stress. Plant HSFs are encoded by large gene families with variable sequences, expression and function. Plant HSFs regulate transcription of a wide range of stress-induced genes, including HSPs and other chaperones, reactive oxygen species scavengers, enzymes involved in protective metabolic reactions and osmolytic biosynthesis, or other transcriptional factors. Genome-wide analysis of Arabidodpsis, rice, poplar, lettuce, and wheat revealed a complex network of interaction between the Hsps and Hsfs gene families that form plant protection against oxidative stress. Plant protection systems are discussed, with special emphasis on the role of HSPs and HSFs in plant responses to stress, which will be useful for the development of technologies to increase productivity and stress resistance of plant crops.

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REFERENCES

  1. Del Río L.A. 2015. ROS and RNS in plant physiology: An overview. J. Exp. Bot. 66, 2827–2837. https://doi.org/10.1093/jxb/erv099

    Article  CAS  PubMed  Google Scholar 

  2. Xia X.J., Zhou Y.H., Shi K., Zhou J., Foyer C.H., Yu J.Q. 2015. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 66, 2839–2856. https://doi.org/10.1093/jxb/erv089

    Article  CAS  PubMed  Google Scholar 

  3. Mittler R. 2017. ROS are good. Trends Plant Sci. 22, 11–19. https://doi.org/10.1016/j.tplants.2016.08.002

    Article  CAS  PubMed  Google Scholar 

  4. Caverzan A., Piasecki C., Chavarria G., Stewart C.N., Jr., Vargas L. 2019. Defenses against ROS in crops and weeds: The effects of interference and herbicides. Int. J. Mol. Sci. 20, 1086. https://doi.org/10.3390/ijms20051086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sewelam N., Kazan K., Hüdig M., Maurino V.G., Schenk P.M. 2019. The AtHSP17.4C1 gene expression is mediated by diverse signals that link biotic and abiotic stress factors with ROS and can be a useful molecular marker for oxidative stress. Int. J. Mol. Sci. 20, 3201. https://doi.org/10.3390/ijms20133201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405– 410. https://doi.org/10.1016/s1360-1385(02)02312-9

    Article  CAS  PubMed  Google Scholar 

  7. Ul Haq S., Khan A., Ali M., Khattak A.M., Gai W.X., Zhang H.X., Wei A.M., Gong Z.H. 2019. Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int. J. Mol. Sci. 20, 5321. https://doi.org/10.3390/ijms20215321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Volkov R.A., Panchuk I.I., Mullineaux P.M., Schöffl F. 2006. Heat stress induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol. 61, 733–746. https://doi.org/10.1007/s11103-006-0045-4

    Article  CAS  PubMed  Google Scholar 

  9. Singh S.S., Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

    Article  CAS  Google Scholar 

  10. Katano K., Kohey Honda K., Suzuki N. 2018. Integration between ROS regulatory systems and other signals in the regulation of various types of heat responses in plants. Int. J. Mol. Sci. 19, 3370. https://doi.org/10.3390/ijms19113370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Scarpeci T.E., Zanor M.I., Valle E.M. 2008. Investigating the role of plant heat shock proteins during oxidative stress. Plant Signal. Behav. 3, 856–857. https://doi.org/10.4161/psb.3.10.6021

    Article  PubMed  PubMed Central  Google Scholar 

  12. Andrási N., Pettkó-Szandtner A., Szabados L. 2021. Diversity of plant heat shock factors: Regulation, interactions, and functions. J. Exp. Bot. 72. 1558–1575. https://doi.org/10.1093/jxb/eraa576

    Article  CAS  PubMed  Google Scholar 

  13. Suzuki N., Koussevitzky S., Mittler R., Miller G. 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x

    Article  CAS  PubMed  Google Scholar 

  14. Yurina N.P., Odintsova M.S. 2019. J. Plant. Physiol. 66, 509–520. https://doi.org/10.1134/S1021443719040149

    Article  CAS  Google Scholar 

  15. Driedonks N., Xu J., Peters J.L., Park S., Rieu I. 2015. Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Front. Plant Sci. 6, 999. https://doi.org/10.1134/S000629791510005310.3389/fpls.2015.00999

  16. Hasanuzzaman M., Bhuyan M.H.M.B., Anee T.I., Parvin K., Nahar K., Mahmud J.A., Fujita M. 2019. Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants. 8, 384. https://doi.org/10.3390/antiox8090384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li Z.Y., Long R.C., Zhang T.J., Yang Q.C., Kang J.M. 2016. Molecular cloning and characterization of the MsHSP17.7 gene from Medicago sativa L. Mol. Biol. Rep. 43, 815–826. https://doi.org/10.1007/s11033-016-4008-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Muthusamy S.K., Dalal M., Chinnusamy V., Bansal K.C. 2017. Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. J. Plant Physiol. 211, 100–113. https://doi.org/10.1016/j.jplph.2017.01.004

    Article  CAS  PubMed  Google Scholar 

  19. Liu J., Pang X., Cheng Y., Yin Y., Zhang Q., Su W., Hu B., Guo Q., Ha S., Zhang J. Wan H. 2018. The Hsp70 gene family in Solanum tuberosum: Genome-wide identification, phylogeny, and expression patterns. Sci. Rep. 8, 16628. https://doi.org/10.1038/s41598-018-34878-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Waters E.R., Vierling E. 2020. Plant small heat shock proteins—evolutionary and functional diversity. New Phytol. 227, 24–37. https://doi.org/10.1111/nph.16536

    Article  CAS  PubMed  Google Scholar 

  21. Wang W., Vinocur B., Shoseyov O., Altman A. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244–252. https://doi.org/10.1016/j.tplants.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  22. Al-Whaibi M.H. 2011. Plant heat-shock proteins: a mini review. J. King Saud Univ.—Science. 23(2), 139–150). https://doi.org/10.1016/j.jksus.2010.06.022

  23. Chen B., Feder M.E., Kang L. 2018. Evolution of heat-shock protein expression underlying adaptive responses to environmental stress. Mol. Ecol. 27, 3040–3054. https://doi.org/10.1134/S000629791510005310.1111/mec.14769

  24. Swindell W.R., Huebner M., Weber A.P. 2007. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics. 8, 125. https://doi.org/10.1186/1471-2164-8-125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hu W., Hu G., Han B. 2009. Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci. 176, 583–590. https://doi.org/10.1016/j.plantsci.2009.01.016

    Article  CAS  PubMed  Google Scholar 

  26. Zhang J., Liu B., Li J., Zhang L., Wang Y., Zheng H., Lu M., Chen J. 2015. Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics. 16, 181. https://doi.org/10.1186/s12864-015-1398-3

    Article  PubMed  PubMed Central  Google Scholar 

  27. Dudrez L., Causse S., Bonan N., Dumetier B. 2020. Heat-shock proteins: chaperoning DNA repair. Oncogene. 39, 516–529. https://doi.org/10.1134/S000629791510005310.1038/s41388-019-1016-y

  28. Rutgers M., Muranaka L.S., Muhlhaus T., Sommer F., Thoms S., Schurig J., Willmund F., Schulz-Raffelt M., Schroda M. 2017. Substrates of the chloroplast small heat shock proteins 22E/F point to thermolability as a regulative switch for heat acclimation in Chlamydomonas reinhardtii. Plant Mol. Biol. 95, 579–591. https://doi.org/10.1134/S000629791510005310.1007/s11103-017-0672-y

  29. Rosenzweig R., Nillegoda N.B., Mayer M.P., Bukau B. 2019. The Hsp70 chaperone network. Nat. Rev. Mol. Cell Biol. 20, 665–680. https://doi.org/10.1038/s41580-019-0133-3

    Article  CAS  PubMed  Google Scholar 

  30. Jiang C., Xu J., Zhang H., Zhang X., Shi J., Li M., Ming F. 2009. A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ. 32, 1046–1059. https://doi.org/10.1111/j.1365-3040.2009.01987.x

    Article  CAS  PubMed  Google Scholar 

  31. Kong F., Deng Y., Wang G., Wang J., Liang X., Meng Q. 2014. LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J. Integr. Plant Biol. 56, 63–74. https://doi.org/10.1111/jipb.12119

    Article  CAS  PubMed  Google Scholar 

  32. Song A., Zhu X., Chen F., Gao H., Jiang J., Chen S. 2014. A chrysanthemum heat shock protein confers tolerance to abiotic stress. Int. J. Mol. Sci. 15, 5063–5078. https://doi.org/10.3390/ijms15035063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wang K., Zhang X., Goatley M., Ervin E. 2014. Heat shock proteins in relation to heat stress tolerance of creeping bentgrass at different N levels. PLoS One. 9 (7), e102914. https://doi.org/10.1371/journal.pone.0102914

  34. Chankova S., Yurina N. 2012. Micro-algae as a model system for studying of genotype resistance to oxidative stress and adaptive response. In Radiobiology and Environmental Security. Mothersill C.E., Korogodina V., Seymour C.B., Eds. Dordrecht: Springer, 19–30.

    Google Scholar 

  35. Chankova S., Mitrovska Z., Miteva D., Oleskina Y.P., Yurina N.P. 2013. Heat shock protein HSP70B as a marker for genotype resistance to environmental stress in Chlorella species from contrasting habitats. Gene. 516, 184–189. https://doi.org/10.1016/j.gene.2012.11.052

    Article  CAS  PubMed  Google Scholar 

  36. Chankova S., Dimova E., Mitrovska Z., Miteva D., Mokerova D., Yonova P., Yurina N. 2014. Antioxidant and HSP70B responses in Chlamydomonas reinhardtii genotypes with different resistance to oxidative stress. Ecotoxicol. Environ. Saf. 101, 131–137. https://doi.org/10.1016/j.ecoenv.2013.11.015

    Article  CAS  PubMed  Google Scholar 

  37. Chankova S.G., Yurina N.P. 2016. Chloroplast heat shock protein 70B as marker of oxidative stress. In Heat Shock Proteins and Plants. Asea A., Kaur P., Calderwood S., Eds. Springer. 10, 169–188. https://doi.org/10.1007/978-3-319-46340-7_9

  38. Fragkostefanakis S., Röth S., Schleiff E., Scharf K.-D. 2015. Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks: Hsfs and Hsps for improvement of crop thermotolerance. Plant Cell Environ. 38, 1881–1895. https://doi.org/10.1111/pce.12396

    Article  CAS  PubMed  Google Scholar 

  39. Tian F., Hu X..-L., Yao T., Yang X., Chen J.-G., Lu M.-Z., Zhang J. 2021. Recent advances in the roles of HSFs and HSPs in heat stress response in woody plants. Front. Plant Sci. 12, 704905. https://doi.org/10.3389/fpls.2021.704905

    Article  PubMed  PubMed Central  Google Scholar 

  40. Liu H., Charng Y. 2013. Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol. 163, 276–290. https://doi.org/10.1104/pp.113.221168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Guo M, Liu J.-H, Ma X., Luo D.-X., Gong Z.-H., Lu M.-H. 2016. The plant heat stress transcription factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Front Plant Sci. 7, 114. https://doi.org/10.3389/fpls.2016.00114

    Article  PubMed  PubMed Central  Google Scholar 

  42. Miller G., Mittler R. 2006. Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279–288. https://doi.org/10.1093/aob/mcl107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Reddy P.S., Kavi Kishor P.B., Seiler C., Kuhlmann M., Eschen-Lippold L., Lee J., Reddy M.K., Sreenivasulu N. 2014. Unraveling regulation of the small heat shock proteins by the heat shock factor HvHsfB2c in barley: its implications in drought stress response and seed development. PLoS One. 9, e89125. https://doi.org/10.1371/journal.pone.0089125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Yang Z., Wang Y., Gao Y., Zhou Y., Zhang E., Hu Y., Yuan Y., Liang G., Xu C. 2014. Adaptive evolution and divergent expression of heat stress transcription factors in grasses. BMC Evol. Biol. 14, 147. https://doi.org/10.1186/1471-2148-14-147

    Article  PubMed  PubMed Central  Google Scholar 

  45. Agarwal P., Khurana P. 2019. Functional characterization of HSFs from wheat in response to heat and other abiotic stress conditions. Funct. Integrat. Genom. 19, 497–513. https://doi.org/10.1007/s10142-019-00666-3

    Article  CAS  Google Scholar 

  46. Zhang H., Li G., Fu C., Duan S., Hu D., Guo X. 2020. Genome-wide identification, transcriptome analysis and alternative splicing events of Hsf family genes in maize. Sci. Rep. 10, 8073. https://doi.org/10.1038/s41598-020-65068-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Jin G.H., Gho H.J., Jung K.H. 2013. A systematic view of rice heat shock transcription factor family using phylogenomic analysis. J. Plant Physiol. 170, 321–329.

    Article  CAS  PubMed  Google Scholar 

  48. Wang X., Shi X., Chen S., Ma C., Xu S. 2018. Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front. Plant Sci. 9, 71.https://doi.org/10.3389/fpls.2018.00071

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lin Y.-X., Jiang H.-Y., Chu Z.-X., Tang X.-L., Zhu S.W., Cheng B.-J. 2011. Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics. 12, 76. https://doi.org/10.1186/1471-2164-12-76

  50. Zhang L., Zhao H.-K., Dong Q.-L., Zhang Y.-Y. Wang Y.-M., Li H.-Y., Xing G.-J., Li Q.-Y., Dong Y.-S. 2015. Genome-wide analysis and expression profiling under heat and drought treatments of HSP70 gene family in soybean (Glycine max L.). Front. Plant Sci. 6, 773. https://doi.org/10.3389/fpls.2015.00773

    Article  PubMed  PubMed Central  Google Scholar 

  51. Scharf K.D., Berberich T., Ebersberger I., Nover L. 2012. The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochim. Biophys. Acta. 1819, 104–119. https://doi.org/10.1016/j.bbagrm.2011.10.002

    Article  CAS  PubMed  Google Scholar 

  52. Zhu J.-K. 2016. Abiotic stress signaling and responses in plants. Cell. 167, 313–324. https://doi.org/10.1016/j.cell.2016.08.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Rejeb I., Pastor V., Mauch-Mani B. 2014. Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants. 3, 458–475. https://doi.org/10.3390/plants3040458

    Article  PubMed  PubMed Central  Google Scholar 

  54. Li P.S., Yu T.F., He G.H., Chen M., Zhou Y.B., Chai S.C., Xu Z.S., Ma Y.Z. 2014. Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement in drought and heat stresses. BMC Genomics. 15, 1009. https://doi.org/10.1186/1471-2164-15-1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Li M., Doll J., Weckermann K., Oecking C., Berendzen K.W., Schöffl F. 2010. Detection of in vivo interactions between Arabidopsis class A-HSFs, using a novel BiFC fragment, and identification of novel class B-HSF interacting proteins. Eur. J. Cell Biol. 89, 126–132. https://doi.org/10.1016/j.ejcb.2009.10.012

    Article  CAS  PubMed  Google Scholar 

  56. Albihlal W.S., Obomighie I., Blein T., Persad R., Chernukhin I., Crespi M., Bechtold U., Mullineaux P.M. 2018. Arabidopsis heat shock transcription factora1b regulates multiple developmental genes under benign and stress conditions. J. Exp. Bot. 69, 2847–2862. https://doi.org/10.1093/jxb/ery142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Qu A.L., Ding Y.F., Jiang Q., Zhu C. 2013. Molecular mechanisms of the plant heat stress response. Biochem. Biophys. Res. Commun. 432, 203–207. https://doi.org/10.1016/j.bbrc.2013.01.104

    Article  CAS  PubMed  Google Scholar 

  58. Ikeda M., Mitsuda N., Ohme-Takagi M. 2011. Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 157, 1243–1254. https://doi.org/10.1104/pp.111.179036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bian X., Li W., Niu C., Wei W., Hu Y., Han J.-Q., Lu X., Tao J.-J., Jin M., Qin H., Zhou B., Wan-Ke Zhang W.-R., Ma B., Wang G.-D., Yu D.-Y., Lai Y.-C., Chen S.-Y., Zhang J.-S. 2020. A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis. New Phytol. 225, 268–283. https://doi.org/10.1111/nph.16104

    Article  CAS  PubMed  Google Scholar 

  60. Zhao J., Lu Z., Wang L., Jin B. 2021. Plant responses to heat stress: Physiology, transcription, noncoding RNAs, and epigenetics. Int. J. Mol. Sci. 22, 117. https://doi.org/10.3390/ijms22010117

    Article  CAS  Google Scholar 

  61. Zhuang L., Cao W., Wang J., Yu J., Yang Z., Huang B. 2018. Characterization and functional analysis of FaHsfC1b from Festuca arundinacea conferring heat tolerance in Arabidopsis. Int. J. Mol. Sci. 19, 2702. https://doi.org/10.3390/ijms19092702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ding Y.L., Shi Y.T., Yang S.H. 2020. Molecular regulation of plant responses to environmental temperatures. Mol. Plant. 13, 544–564. https://doi.org/10.1016/j.molp.2020.02.004

    Article  CAS  PubMed  Google Scholar 

  63. Schmidt R., Schippers J.H.M., Welker A., Mieulet D., Guiderdoni E., Mueller-Roeber B. 2012. Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica. AoB PLANTS. pls011. https://doi.org/10.1093/aobpla/pls011

  64. Xue G.P., Sadat S., Drenth J., Mcintyre C.L. 2014. The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. J. Exp. Bot. 65, 539–557. https://doi.org/10.1093/jxb/ert399

    Article  CAS  PubMed  Google Scholar 

  65. Huang X.Y., Tao P., Li B.Y., Wang W.H., Yue Z.C., Lei J.L., Zhong X.M. 2015. Genome-wide identification, classification, and analysis of heat shock transcription factor family in Chinese cabbage (Brassica rapa pekinensis). Genet. Mol. Res. 14, 2189–2204. https://doi.org/10.4238/2015

    Article  PubMed  Google Scholar 

  66. Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L., Scharf K.D. 2002. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555–1567. https://doi.org/10.1101/gad.228802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Yoshida T., Ohama N., Nakajima J., Kidokoro S., Mi-zoi J., Nakashima K., Maruyama K., Kim J.-M., Seki M., Todaka D., Osakabe Y., Sakuma Y., Schöffl F., Shinozaki K., Yamaguchi-Shinozaki K. 2011. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock responsive gene expression. Mol. Genet. Genom. 286, 321–332. https://doi.org/10.1007/s00438-011-0647-7

    Article  CAS  Google Scholar 

  68. Li X.D., Wang X.L., Cai Y.M., Wu J.H., Mo B.T., Yu E.R. 2017. Arabidopsis heat stress transcription factors A2 (HSFA2) and A3 (HSFA3) function in the same heat regulation pathway. Acta Physiol. Plantarum. 39, 39–67. https://doi.org/10.1007/s11738-017-2351-7

    Article  CAS  Google Scholar 

  69. Singh A., Mittal D., Lavania D., Agarwal M., Mishra R.C., Grover A. 2012. OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress Chaperones. 17, 243–254. https://doi.org/10.1007/s12192-011-0303-5

    Article  CAS  PubMed  Google Scholar 

  70. Nishizawa A., Yabuta Y., Yoshida E., Maruta T., Yoshimura K., Shigeoka S. 2006. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535–547. https://doi.org/10.1111/j.1365-313X.2006.02889.x

    Article  CAS  PubMed  Google Scholar 

  71. Yoshida T., Sakuma Y., Todaka D. Maruyama K., Qin F., Mizoi J., Kidokoro S., Fujita Y., Shinozaki K., Yamaguchi-Shinozaki K. 2008. Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem. Biophys. Res. Commun. 368, 515–521. https://doi.org/10.1016/j.bbrc.2008.01.134

    Article  CAS  PubMed  Google Scholar 

  72. Huang H.Y., Chang K.Y., Wu S.J. 2018. High irradiance sensitive phenotype of Arabidopsis hit2/xpo1a mutant is caused in part by nuclear confinement of AtHsfA4a. Biol. Plantarum. 62, 69–79. https://doi.org/10.1007/s10535-017-0753-4

    Article  CAS  Google Scholar 

  73. Andrási N., Rigó G., Zsigmond L., Pérez-Salamó I., Papdi C., Klement E., Pettkó-Szandtner A., Baba A.I., Ayaydin F., Dasari R., Cséplő A., Szabados L. 2019. The mitogen-activated protein kinase 4-phosphorylated heat shock factor A4A regulates responses to combined salt and heat stresses. J. Exp. Botany. 70, 4903–4918. https://doi.org/10.1093/jxb/erz217

    Article  CAS  Google Scholar 

  74. Pérez-Salamó I., Papdi C., Rigó G., Zsigmond L., Vilela B., Lumbreras V., Nagy I., Horváth B., Domoki M., Darula Z., Medzihradszky K., Bögre L., Koncz C., Szabados L. 2014. The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol. 165, 319–334. https://doi.org/10.1104/pp.114.237891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Zhu M.D., Zhang M., Gao D.J., Zhou K., Tang S.J., Zhou B., Lv Y.M. 2020. Rice OsHSFA3 gene improves drought tolerance by modulating polyamine biosynthesis depending on abscisic acid and ROS levels. Int. J. Mol. Sci. 21, 1857. https://doi.org/10.3390/ijms21051857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lang S., Liu X., Xue H., Li X., Wang X. 2017. Functional characterization of BnHSFA4a as a heat shock transcription factor in controlling the re-establishment of desiccation tolerance in seeds. J. Exp. Bot. 68, 2361–2375. https://doi.org/10.1093/jxb/erx097

    Article  CAS  PubMed  Google Scholar 

  77. Busch W., Wunderlich M., Schöffl F. 2005. Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41, 1–14. https://doi.org/10.1111/j.1365-313X.2004.02272.x

    Article  CAS  PubMed  Google Scholar 

  78. Schramm F., Ganguli A., Kiehlmann E., Englich G., Walch D., von Koskull-Döring P. 2006. The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 60, 759–772. https://doi.org/10.1007/s11103-005-5750-x

    Article  CAS  PubMed  Google Scholar 

  79. Giesguth M., Sahm A., Simon S., Dietz K.J. 2015. Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett. 589, 718–725. https://doi.org/10.1016/j.febslet.2015.01.039

    Article  CAS  PubMed  Google Scholar 

  80. Li H.C., Zhang H.N., Li G.L., Liu Z.H., Zhang Y.M., Zhang H.M., Guo X.L. 2015. Expression of maize heat shock transcription factor gene ZmHsf06 enhances the thermotolerance and drought-stress tolerance of transgenic Arabidopsis. Funct. Plant Biol. 42, 1080–1091. https://doi.org/10.1071/FP15080

    Article  CAS  PubMed  Google Scholar 

  81. Chen S., Yu M., Li H., Wang H., Lu Z., Zhang Y., Liu M. et al. 2020. SaHsfA4c from Sedum alfredii Hance enhances cadmium tolerance by regulating ROS-scavenger activities and heat shock proteins expression. Front. Plant Sci. 11, 142. https://doi.org/10.3389/fpls.2020.00142

    Article  PubMed  PubMed Central  Google Scholar 

  82. Banti V., Loreti E., Novi G., Santaniello A., Alpi A., Perata P. 2008. Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ. 31, 1029–1037. https://doi.org/10.1111/j.1365-3040.2008.01816.x

    Article  CAS  PubMed  Google Scholar 

  83. Hu Y., Mesihovic A., Jiménez-Gómez J.M., Röth S., Gebhardt P., Bublak D., Bovy A., Scharf K.D., Schleiff E., Fragkostefanakis S. 2020. Natural variation in HsfA2 pre-mRNA splicing is associated with changes in thermotolerance during tomato domestication. New Phytologist. 225, 1297–1310. https://doi.org/10.1111/nph.16221

    Article  CAS  PubMed  Google Scholar 

  84. Bigeard J., Hirt H. 2018. Nuclear signaling of plant MAPKs. Front. Plant Sci. 9, 469. https://doi.org/10.3389/fpls.2018.00469

    Article  PubMed  PubMed Central  Google Scholar 

  85. Evrard A., Kumar M., Lecourieux D., Lucks J., von Koskull-Döring P., Hirt H. 2013. Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. Peer J. 1, e59. https://doi.org/10.7717/peerj.59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Rytz T.C., Miller M.J., McLoughlin F., Augustine R.C., Marshall R.S., Juan Y.T., Charng Y.Y., Scalf M., Smith L.M., Vierstra R.D. 2018. SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress. Plant Cell. 30, 1077–1099. https://doi.org/10.1105/tpc.17.00993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Liu J., Feng L., Li J., He Z. 2015. Genetic and epigenetic control of plant heat responses. Front. Plant Sci. 6, 267. https://doi.org/10.3389/fpls.2015.00267

    Article  PubMed  PubMed Central  Google Scholar 

  88. Xu Y., Zhang S., Lin S., Guo Y., Deng W., Zhang Y., Xue Y. 2017. WERAM: A database of writers, erasers and readers of histone acetylation and methylation in eukaryotes. Nucleic Acids Res. 45, D264–D270. https://doi.org/10.1093/nar/gkw1011

    Article  CAS  PubMed  Google Scholar 

  89. Lämke J., Brzezinka K., Altmann S., Bäurle I. 2016. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 35, 162–175. https://doi.org/10.15252/embj.201592593

    Article  CAS  PubMed  Google Scholar 

  90. He Y., Li Z. 2018. Epigenetic environmental memories in plants: establishment, maintenance, and reprogramming. Trends Genet. 34, 856–866. https://doi.org/10.1016/j.tig.2018.07.006

    Article  CAS  PubMed  Google Scholar 

  91. Liu H.C., Lämke J., Lin S.Y., Hung M.J., Liu K.M., Charng Y.Y., Bäurle I. 2018. Distinct heat shock factors and chromatin modifications mediate the organautonomous transcriptional memory of heat stress. Plant J. 95, 401–413. https://doi.org/10.1111/tpj.13958

    Article  CAS  PubMed  Google Scholar 

  92. Stief A., Brzezinka K., Lämke J., Bäurle I. 2014. Epigenetic responses to heat stress at different time scales and the involvement of small RNAs. Plant Signal. Behav. 9, e970430. https://doi.org/10.4161/15592316.2014.970430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Singh R.K., Jaishankar J., Muthamilarasan M., Shweta S., Dangi A., Prasad M. 2016. Genome-wide analysis of heat shock proteins in C4 model, foxtail millet identifies potential candidates for crop improvement under abiotic stress. Sci. Rep. 6, 32641, https://doi.org/10.1038/srep32641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kim T., Samraj S., Jiménez J., Gómez C., Liu T., Begcy K. 2021. Genome-wide identification of heat shock factors and heat shock proteins in response to UV and high intensity light stress in lettuce. BMC Plant Biol. 17, 185. https://doi.org/10.1186/s12870-021-02959-x

    Article  CAS  Google Scholar 

  95. Kumar A., Sharma S., Chunduri V., Kaur A., Kaur S., Malhotra N., Kumar A., Kapoor P., Kumari A., Kaur J., Sonah H., Garg M. 2020. Genome-wide identification and characterization of heat shock protein family reveals role in and stress conditions in Triticum aestivum L. Sci. Rep. 10, 7858. https://doi.org/10.1038/s41598-020-64746-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Duan S., Liu B., Zhang Y., Li G., Guo X. 2019. Genome-wide identification and abiotic stress-responsive pattern of heat shock transcription factor family in Triticum aestivum L. BMC Genomics. 20, 257. https://doi.org/10.1186/s12864-019-5617-1

    Article  PubMed  PubMed Central  Google Scholar 

  97. Huang J., Hai Z., Wang R., Yu Y., Chen X., Liang W., Wang H. 2022 . Genome-wide analysis of HSP20 gene family and expression patterns under heat stress in cucumber (Cucumis sativus L.). Front. Plant. Sci. 13, 968418. https://doi.org/10.3389/fpls.2022.968418

    Article  PubMed  PubMed Central  Google Scholar 

  98. Hu Y., Zhang T., Liu Y., Li Y., Wang M., Zhu B., Liao D., Yun T., Huang W., Wen Zhang W., Yang Zhou Y. 2021. Pumpkin (Cucurbita moschata) HSP20 gene family identification and expression under heat stress. Front. Genet. 12, 753953. https://doi.org/10.1134/S000629791510005310.3389/fgene.2021.753953

  99. Metzger D.C.H., Hemmer-Hansen J., Schulte P.M. 2016. Conserved structure and expression of Hsp70 paralogs in teleost fishes. Comp. Biochem. Physiol., Part D: Genomics Proteomics. 18, 10–20. https://doi.org/10.1016/j.cbd.2016.01.007

    Article  CAS  PubMed  Google Scholar 

  100. Tang T., Yu A., Li P., Yang H., Liu G., Liu L. 2016. Sequence analysis of the Hsp70 family in moss and evaluation of their functions in abiotic stress responses. Sci. Rep. 6, 33650. https://doi.org/10.1038/srep33650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Liu J., Wang R., Liu W., Zhang H., Guo Y., Wen R. 2018. Genome-wide characterization of heat-shock protein 70s from Chenopodium quinoa and expression analyses of Cqhsp70s in response to drought stress. Genes (Basel). 9, 35. https://doi.org/10.3390/genes9020035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Su H., Xing M., Liu X., Fang Z., Yang L., Zhuang M., Zhang Y., Wang Y., Lv H. 2019. Genome-wide analysis of HSP70 family genes in cabbage (Brassica oleracea var. capitata) reveals their involvement in floral development. BMC Genomics. 20, 369. https://doi.org/10.1186/s12864-019-5757-3

    Article  PubMed  PubMed Central  Google Scholar 

  103. Rowarth N.M., Dauphinee A.N., Denbigh G.L., Gunawardena A.H. 2020. Hsp70 plays a role in programmed cell death during the remodelling of leaves of the lace plant (Aponogeton madagascariensis). J. Exp. Bot. 71, 907–918. https://doi.org/10.1093/jxb/erz447

    Article  CAS  PubMed  Google Scholar 

  104. Schroda M., Vallon O., Wollman F.-A., Beck C.F. 1999. A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell. 11, 1165–1178. https://doi.org/10.1105/tpc.11.6.1165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Chen Y., Chen X., Wang H., Bao Y., Zhang W. 2014. Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. Proteome Sci. 12, 33. https://doi.org/10.1186/1477-5956-12-33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Yu L., Wang W., Zeng S., Chen Z., Yang A., Shi J., Zhao X., Song B. 2018. Label-free quantitative proteomics analysis of cytosinpeptidemycin responses in Southern rice black-streaked dwarf virus-infected rice. Pestic. Biochem. Physiol. 147, 20–26. https://doi.org/10.1016/j.pestbp.2017.06.005

    Article  CAS  PubMed  Google Scholar 

  107. Lavania D., Dhingra A., Siddiqui M.H., Al-Whaibi M.H., Grover A. 2015. Current status of the production of high temperature tolerant transgenic crops for cultivation in Warmer Climates. Plant Physiol. Biochem. 86, 100–108. https://doi.org/10.1016/j.plaphy.2014.11.019

    Article  CAS  PubMed  Google Scholar 

  108. Rochaix J.-D. 2022. Chloroplast protein import machinery and quality control. FEBS J. 289, 6908–6918. https://doi.org/10.1111/febs.16464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Suzuki N. 2023. Fine tuning of ROS, redox and energy regulatory systems associated with the functions of chloroplasts and mitochondria in plants under heat stress. Int. J. Mol. Sci. 24, 1356. https://doi.org/10.3390/ijms24021356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Zhu X., Huang C., Zhang L., Liu H., Yu J., Hu Z., Hua W. 2017. Systematic analysis of HsF family genes in the Brassica napus genome reveals novel responses to heat, drought and high CO2 stresses. Front. Plant Sci. 8, 1174. https://doi.org/10.3389/fpls.2017.01174

    Article  PubMed  PubMed Central  Google Scholar 

  111. Mishra D., Shekhar S., Singh D., Chakraborty S., Chakrabort N. 2018. Heat shock proteins and abiotic stress tolerance in plants. In Regulation of Heat Shock Protein Responses, Heat Shock Proteins. 13, 41–69. https://doi.org/10.1007/978-3-319-74715-6_3

  112. Lohani N., Jain D., Singh M.B., Bhalla P.L. 2020. Engineering multiple abiotic stress tolerance in Canola, Brassica napus. Front. Plant Sci. 11, 3. https://doi.org/10.3389/fpls.2020.00003

    Article  PubMed  PubMed Central  Google Scholar 

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The study was supported by the Russian Science Foundation (grant no. 2324 00486).

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  1. Bach Institute of Biochemistry, Fundamentals of Biotechnology Federal Research Center, Russian Academy of Sciences, 119071, Moscow, Russia

    N. P. Yurina

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Abbreviations: HSPs, heat shock proteins; HSFs, transcription factors of heat shock proteins genes; TF, transcription factor.

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Yurina, N.P. Heat Shock Proteins in Plant Protection from Oxidative Stress. Mol Biol 57, 951–964 (2023). https://doi.org/10.1134/S0026893323060201

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