МАМР-индуцируемый иммунитетPTI-индуцируемый иммунитетбелки теплового шокаврожденный иммунитетиммунитет растенийстрессовые белкиМинистерство науки и высшего образования Российской ФедерацииMinistry of Science and Higher Education of the Russian Federation122041100050-61.Lindquist S. The heat-shock response // Annu. Rev. Biochem. 1986. V. 55. P. 1151. https://doi.org/10.1146/annurev.bi.55.070186.0054432.Lindquist S., Craig E.A. The heat-shock proteins // Annu. Rev. Genet. 1988. V. 22. P. 631. https://doi.org/10.1146/annurev.ge.22.120188.0032153.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. V. 9. P. 244. https://doi.org/10.1016/j.tplants.2004.03.0064.Carra S., Alberti S., Arrigo P.A., Benesch J.L., Benjamin I.J., Boelens W., Bartelt-Kirbach B., Brundel B.J.J.M., Buchner J., Bukau B., Carver J.A., Ecroyd H., Emanuelsson C., Finet S., Golenhofen N. et al. The growing world of small heat shock proteins: from structure to functions // Cell Stress Chaperones. 2017. V. 22. P. 601. https://doi.org/10.1007/s12192-017-0787-85.Whitley D., Goldberg S.P., Jordan W.D. Heat shock proteins: a review of the molecular chaperones // J. Vasc. Sur. 1999. V. 29. P. 748. https://doi.org/10.1016/s0741-5214(99)70329-06.Sitia R., Braakman I. Quality control in the endoplasmic reticulum protein factory // Nature. 2003. V. 426. P. 881. https://doi.org/10.1038/nature022627.Войников В.К., Иванова Г.Г., Рудиковский А.В. Белки теплового шока // Физиология растений. 1984. Т. 31. С. 970.8.Nover L. The heat shock response. London: Taylor & Francis, 1991. 153 p.9.Vierling E. The roles of heat shock proteins in plants // Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991. V. 42. P. 579. https://doi.org/10.1146/annurev.pp.42.060191.00305110.Kidwai M., Singh P., Dutta P., Chawda K., Chakrabarty D. Molecular mechanisms of heat shock proteins for sustainable plant growth and production // Harsh environment and plant resilience / Eds. A. Husen. Springer. 2021. P. 141. https://doi.org/10.1007/978-3-030-65912-7_711.Boston R.S., Viitanen P.V., Vierling E. Molecular chaperones and protein folding in plants // Plant Mol. Biol. 1996. V. 32. P. 191. https://doi.org/10.1007/BF0003938312.Al-Whaibi M.H. Plant heat-shock proteins: a mini review // J. King Saud Univ. Sci. 2011. V. 23. P. 139. https://doi.org/10.1016/j.jksus.2010.06.02213.Kaura V., Malhotra P.K., Mittal A., Sanghera G.S., Kaur N., Bhardwaj R.D., Cheema R.S., Kaur G. Physiological, biochemical, and gene expression responses of sugarcane under cold, drought and salt stresses // J. Plant Growth Regul. 2023. V. 42. P. 6367. https://doi.org/10.1007/s00344-022-10850-814.Kim T., Samraj S., Jiménez J., Gómez C., Liu T., Begcy K. Genome-wide identifcation of heat shock factors and heat shock proteins in response to UV and high intensity light stress in lettuce // BMC Plant Biol. 2021. V. 21. P. 185. https://doi.org/10.1186/s12870-021-02959-x15.Chaudhary R., Baranwal V.K., Kumar R., Sircar D., Chauhan H. Genomewide identifcation and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development // Funct. Integr. Genom. 2019. V. 19. P. 1007. https://doi.org/10.1007/s10142-019-00695-y16.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 Genomics. 2007. V. 8. P. 125. https://doi.org/10.1186/1471-2164-8-12517.Aghaie P., Tafreshi S.A.H. Central role of 70-kDa heat shock protein in adaptation of plants to drought stress // Cell Stress Chaperones. 2020. V. 25. P. 1071. https://doi.org/10.1007/s12192-020-01144-718.Chatterjee A., Galiba G., Kocsy G., Kumar R., Dey N. Molecular insight into drought tolerance of CR Dhan 40: an upland rice line from Eastern India // J. Crop Sci. Biotechnol. 2023. https://doi.org/10.1007/s12892-023-00222-319.Bishnoi A., Jangir P., Shekhawat P.K., Ram H., Soni P. Silicon supplementation as a promising approach to induce thermotolerance in plants: current understanding and future perspectives // J. Soil Sci. Plant Nutr. 2023. V. 23 P. 34. https://doi.org/10.1007/s42729-022-00914-920.Рихванов Е.Г., Варакина H.Н., Русалева Т.М., Раченко Е.И., Войников В.К. Действие малоната натрия на термотолерантность дрожжей // Микробиология. 2003. Т. 72. С. 616. https://doi.org/10.1023/A:102608701557021.Fares M.A. The evolution of protein moonlighting: adaptive traps and promiscuity in the chaperonins // Biochem. Soc. Trans. 2014. V. 42. P. 1709. https://doi.org/ 10.1042/BST2014022522.Henderson B., Martin A.C. Protein moonlighting: a new factor in biology and medicine // Biochem. Soc. Trans. 2014. V. 42. P. 1671. https://doi.org/10.1042/BST2014027323.Li Z., Menoret A., Srivastava P. Roles of heat-shock proteins in antigen presentation and cross-presentation // Curr. Opin. Immunol. 2002. V. 14. P. 45. https://doi.org/10.1016/s0952-7915(01)00297-724.Wallin R.P., Lundqvist A., More S.H., Von Bonin A., Kiessling R., Ljunggren H.G. Heat-shock proteins as activators of the innate immune system // Trends Immunol. 2002. V. 23. P. 130. https://doi.org/10.1016/S1471-4906(01)02168-825.Tsan M.F., Gao B. Heat shock proteins and immune system // J. Leukoc. Biol. 2009. V. 85. P. 905. https://doi.org/10.1189/jlb.010900526.Ohashi K., Burkart V., Flohe S., Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex // J. Immunol. 2000. V. 164. P. 558. https://doi.org/10.1189/jlb.010900527.Vabulas R.M., Ahmad-Nejad P., da Costa C., Miethke T., Kirschning C.J., Hacker H., Wagner H. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells // J. Biol. Chem. 2001. V. 276. P. 31332. https://doi.org/10.1074/jbc.M10321720028.Maimbo M., Ohnishi K., Hikichi Y., Yoshioka H., Kiba A. Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum // Plant Physiol. 2007. V. 145. P. 1588. https://doi.org/10.1104/pp.107.10535329.Park Ch.-J., Seo Y.-S. Heat shock proteins: a review of the molecular chaperones for plant immunity // Plant Pathol. J. 2015. V. 31. P. 323. https://doi.org/10.5423/PPJ.RW.08.2015.015030.Szatmári Á. Zvara Á., Móricz Á.M., Besenyei E., Szabó E., Ott P.G., Puskás L.G., Bozsó Z. Pattern triggered immunity (PTI) in tobacco: isolation of activated genes suggests role of the phenylpropanoid pathway in inhibition of bacterial pathogens // PLoS ONE. 2014. V. 9. P. e102869. https://doi.org/10.1371/journal.pone.010286931.Ceylan, Y., Altunoglu, Y.C., Horuz, E. HSF and Hsp Gene Families in sunflower: a comprehensive genome-wide determination survey and expression patterns under abiotic stress conditions // Protoplasma. 2023. V. 260. P. 1473. https://doi.org/10.1007/s00709-023-01862-632.Панасенко О.О., Ким М.В., Гусев Н.В. Структура и свойства малых белков теплового шока // Успехи биологической химии. 2003. Т. 42. С. 59.33.Gupta D., Tuteja N. Chaperones and foldases in endoplasmic reticulum stress signaling in plants // Plant Signal. Behav. 2011. V. 6. P. 232. https://doi.org/10.4161/psb.6.2.1549034.Van Ooijen G., Lukasik E., Van Den Burg H.A., Vossen J.H., Cornelissen B.J.C., Takken F.L.W. The small heat shock protein 20 RSI2 interacts with and is required for stability and function of tomato resistance protein I-2 // Plant J. 2010. V. 63. P. 563. https://doi.org/10.1111/j.1365-313X.2010.04260.x35.Zuluaga A.P., Solé M., Lu H., Gongora-Castillo E. Transcriptome responses to Ralstonia solanacearum infection in the roots of the wild potato Solanum commersonii // BMC Genom. 2015. V. 16. P. 246. https://doi.org/10.1186/s12864-015-1460-136.Pan X., Zhu B., Luo Y., Fu D. Unraveling the protein network of tomato fruit in response to necrotrophic phytopathogenic Rhizopus nigricans // PLoS ONE. 2013. V. 8: e73034. https://doi.org/10.1371/journal.pone.007303437.Garofalo C.G., Garavaglia. B.S., Dunger G., Gottig N., Orellano E.G., Ottado J. Expression analysis of small heat shock proteins during compatible and incompatible plant-pathogen interactions // Adv. Stud. Biol. 2009. V. 5. P. 197.38.Ahmed A.A., Pedersen C., Schultz-Larsen T., Kwaaitaal M., Jørgensen H.J.L., Thordal-Christensen H. The barley powdery mildew candidate secreted effector protein CSEP0105 inhibits the chaperone activity of a small heat shock protein // Plant Physiol. 2015. V. 168. P. 321. https://doi.org/10.1104/pp.15.0027839.Kampinga H.H., Craig E.A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity // Nat. Rev. 2010. V. 11. P. 579. https://doi.org/10.1038/nrm294140.Liu J.Z., Whitham S.A. Overexpression of a soybean nuclear localized type-III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance // Plant J. 2013. V. 74. P. 110. https://doi.org/10.1111/tpj.1210841.Hafrén A., Hofius D., Rönnholm G., Sonnewald U., Mäkinen K. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions // Plant Cell. 2010. V. 22. P. 523. https://doi.org/10.1105/tpc.109.07241342.Hofius D., Maier A.T., Dietrich C., Jungkunz I., Bornke F., Maiss E., Sonnewald U. Capsid protein-mediated recruitment of host DnaJ-like proteins is required for Potato virus Y infection in tobacco plants // J. Virol. 2007. V. 81. P. 11870. https://doi.org/10.1128/JVI.01525-0743.Soellick T., Uhrig J.F., Bucher G.L., Kellmann J.W., Schreier P.H. The movement protein NSm of tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins // Proc. Natl. Acad. Sci. USA. 2000. V. 97. P. 2373. https://doi.org/10.1073/pnas.03054839744.Sarkar N.K., Kundnani P., Grover A. Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa) // Cell Stress Chaperones. 2013. V. 18. P. 427. https://doi.org/10.1007/s12192-012-0395-645.Mayer M., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism // Cell. Mol. Life Sci. 2005. V. 62. P. 670. https://doi.org/10.1007/s00018-004-4464-646.Bush G.L., Meyer D.I. The refolding activity of theyeast heat shock proteins Ssa1 and Ssa2 defines their roles in protein translocation // J. Cell Biol. 1996. V. 135. P. 1229. https://doi.org/10.1083/jcb.135.5.122947.Pratt W.B., Toft D.O. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery // Exp. Biol. Med. 2003. V. 228. P. 111. https://doi.org/10.1177/15353702032280020148.Duan Y.H., Guo J., Ding K., Wang S.-J., Zhang H., Dai X.-W., Chen Y.-Y., Govers F., Huang L.-L., Kang Z.-S. Characterization of a wheat Hsp70 gene and its expression in response to stripe rust infection and abiotic stresses // Mol. Biol. Rep. 2011. V. 38. P. 301. https://doi.org/10.1007/s11033-010-0108-049.Kallamadi P.R., Dandu K., Kirti P.B., Rao C. M., Thakur S., Mulpuri S. An insight into powdery mildew-infected, susceptible, resistant and immune sunflower genotypes // Proteomics. 2018. V. 18: 1700418. https://doi.org/10.1002/pmic.20170041850.Yun Z., Gao H., Liu P., Liu S., Luo T., Jin S., Xu Q., Xu J., Cheng Y., Deng X. Comparative proteomic and metabolomic profiling of citrus fruit with enhancement of disease resistance by postharvest heat treatment // BMC Plant Biol. 2013. V. 13. P. 44. https://doi.org/10.1186/1471-2229-13-4451.Byth-Illing H.-A., Bornman L. Heat shock, with recovery, promotes protection of Nicotiana tabacum during subsequent exposure to Ralstonia solanacearum // Cell Stress Chaperones. 2014. V. 19. P. 193. https://doi.org/10.1007/s12192-013-0445-852.Kawano Y., Akamatsu A., Hayashi K., Housen Y., Okuda J., Yao A., Nakashima A., Takahashi H., Yoshida H., Wong H.L., Kawasaki T., Shimamoto K. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity // Cell Host Microbe. 2010. V. 7. P. 362. https://doi.org/10.1016/j.chom.2010.04.01053.Hwang J.R., Zhang C., Patterson C. C-terminus of heat shock protein 70-interacting protein facilitates degradation of apoptosis signal-regulating kinase 1 and inhibits apoptosis signal-regulating kinase 1-dependent apoptosis // Cell Stress Chaperones. 2005. V. 10. P. 147. https://doi.org/10.1379/csc-90r.154.Jung KH., Gho HJ., Nguyen M.X., Kim S.-R., An G. Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress // Funct. Integr. Genomics. 2013. V. 13. P. 391. https://doi.org/10.1007/s10142-013-0331-655.Saijo Y. ER quality control of immune receptors and regulators in plants // Cell Microbiol. 2010. V. 12. P. 716. https://doi.org/10.1111/j.1462-5822.2010.01472.x56.Eichmann R., Schafer P. The endoplasmic reticulum in plant immunity and cell death // Front. Plant Sci. 2012. V. 3. P. 200. https://doi.org/10.3389/fpls.2012.0020057.Fradin E.F., Zhang Z., Ayala J.C.J., Castroverde C.D., Nazar R.N., Robb J., Liu C.-M., Thomma B.P.H.J. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1 // Plant Physiol. 2009. V. 150. P. 320. https://doi.org/10.1104/pp.109.13676258.Stergiopoulos I., de Wit P.J.G.M. Fungal effector proteins // Annu. Rev. Phytopathol. 2009. V. 47. P. 233. https://doi.org/10.1146/annurev.phyto.112408.13263759.Song Y., Zhang Zh., Boshoven J.C., Rovenich H., Seidl M.F., Jakše J., Maruthachalam K., Liu C.-M., Subbarao K.V., Javornik B., Thomma B.P.H.J. Tomato immune receptor Ve1 recognizes surface-exposed co-localized N- and C-termini of Verticillium dahliae effector Ave1 // bioRxiv 103473. 2017. https://doi.org/10.1101/10347360.Schott A., Ravaud S., Keller S., Radzimanowski J., Viotti C., Hillmer S., Sinning I., Strahl S. Arabidopsis stromal-derived Factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum // J. Biol. Chem. 2010. V. 285. P. 18113. https://doi.org/10.1074/jbc.M110.11717661.Liu J.X., Howell S.H. Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants // Plant Cell. 2010. V. 22. P. 2930. https://doi.org/10.1105/tpc.110.07815462.Liebrand T.W.H., Kombrink A., Zhang Z., Sklenar J., Jones A.M.E., Robatzek Z., Thomma B.P.H.J., Joosten M.H.A.J. Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium // Mol. Plant Pathol. 2014. V. 15. P. 109. https://doi.org/10.1111/mpp.1207163.Vu N.T., Kamiya K., Fukushima A., Hao S., Ning W., Arizumi T., Ezura H., Kusano M. Comparative co-expression network analysis extracts the SlHSP70 gene affecting to shoot elongation of tomato // Plant Biotechnol. 2019. V. 36. P. 143. https://doi.org/10.5511/plantbiotechnology.19.0603a64.Muthusamy S.K., Pushpitha P., Makeshkumar T., Sheela M.N. Genome-wide identification and expression analysis of Hsp70 family genes in Cassava (Manihot esculenta Crantz) // Biotech. 2023. V. 13. P. 341. https://doi.org/10.1007/s13205-023-03760-365.Thao N.P., Chen L., Nakashima A., Hara S., Umemura K., Takahashi A., Shirasu K., Kawasaki T., Shimamoto K. RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rise // Plant Cell. 2007. V. 19. P. 4035. https://doi.org/10.1105/tpc.107.05551766.Shirasu K. The HSP90-SGT1 chaperone complex for NLR immune sensors // Annu. Rev. Plant Biol. 2009. V. 60. P. 139. https://doi.org/0.1146/annurev.arplant.59.032607.09290667.Yuan C., Li Ch., Zhao X., Yan C., Wang J., Mou Y., Sun Q., Shan Sh. Genome-wide identification and characterization of HSP90-RAR1-SGT1-Complex members from Arachis genomes and their responses to biotic and abiotic stresses // Front. Genet. 2021. V. 12. P. 689669. https://doi.org/10.3389/fgene.2021.68966968.Seo Y.S., Lee S.K., Song M.Y., Suh J.-P., Hahn T.-R., Ponald P., Jeon J.-S. The HSP90-SGT1-RAR1 molecular chaperone complex: a core modulator in plant immunity // J. Plant Biol. 2008. V. 51. P. 1. https://doi.org/10.1007/BF0303073469.Catlett M.G., Kaplan K.B. Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p // J. Biol. Chem. 2006. V. 281. P. 33739. https://doi.org/ 10.1074/jbc.M60384720070.Xu Z.S., Li Z.Y., Chen Y., Chen M., Li L.C., Ma Y.Z. Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses // Int. J. Mol. Sci. 2012. V. 13. P. 15706. https://doi.org/10.3390/ijms13121570671.Cheng Y.T., Li Y., Huang S., Huang Y., Dong X., Zhang Y., Li X. Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box(SCF)-mediated protein degradation // Proc. Natl. Acad. Sci. USA. 2011. V. 108. P. 14694. https://doi.org/10.1073/pnas.110568510872.Hong S.W., Vierling E. Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress // Plant J. 2001. V. 27. P. 25. https://doi.org/10.1046/j.1365-313x.2001.01066.x73.Lee U., Rioflorido I., Hong S.W., Larkindale J., Waters E.R., Vierling E. The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development // Plant J. 2007. V. 49. P. 115. https://doi.org/10.1111/j.1365-313X.2006.02940.x74.Kreis E., Niemeyer J., Merz M., Scheuring D., Schroda M. CLPB3 is required for the removal of chloroplast protein aggregates and thermotolerance in Chlamydomonas // J. Exp. Bot. 2023. V. 74. P. 3714. https://doi.org/10.1093/jxb/erad10975.Tonsor S.J., Scott C., Boumaza I., Liss T.R., Brodsky J.L., Vierling E. Heat shock protein 101 effects in Arabidopsis thaliana: genetic variation, fitness and pleiotropy in controlled temperatory conditions // Mol. Ecol. 2008. V. 17. P. 1614. https://doi.org/10.1111/j.1365-294X.2008.03690.x76.McLoughlin F., Kim M., Marshall R.S., Vierstra R.D., Vierling E. HSP101 interacts with the proteasome and promotes the clearanceof ubiquitylated protein aggregates // Plant Physiol. 2019. V. 180. P. 1829. https://doi.org/10.1104/pp.19.0026377.Шафикова Т.Н., Омеличкина Ю.В., Солдатенко А.С., Еникеев А.Г., Копытина Т.В., Русалева Т.М., Волкова О.Д. Трансформированная геном hsp101 культура клеток табака обладает повышенной выживаемостью при заражении Clavibacter michiganensis ssp. sepedonicus // Доклады Академии наук. 2013. Т. 450. С. 621. https://doi.org/10.7868/S086956521317027178.Omelichkina Y.V., Boyarkina S.V., Shafikova T.N. Effector-activated immune responses in potato and tobacco cell cultures caused by phytopathogen Clavibacter michiganensis ssp. sepedonicus // Russ. J. Plant Physiol. 2017. V. 64. P. 423. https://doi.org/10.1134/S1021443717020091