Heat shock proteins 70 (HSP70s) are steadily gaining more attention in the field of plant biotic interactions. Though their regulation and activity in plants are much less well characterized than are those of their counterparts in mammals, accumulating evidence indicates that the role of HSP70-mediated defense mechanisms in plant cells is indispensable. In this review, we summarize current knowledge of HSP70 post-translational control in plants. We comment on the phytohormonal regulation of HSP70 expression and protein abundance, and identify a prominent role for cytokinin in HSP70 control. We outline HSP70s' subcellular localizations, chaperone activity, and chaperone-mediated protein degradation. We focus on the role of HSP70s in plant pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity, and discuss the contribution of different HSP70 subfamilies to plant defense against pathogens.

Department of Molecular Biology and Radiobiology Faculty of AgriSciences Mendel University in Brno CZ 61300 Brno Czech Republic

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Abdul Malik NA, Kumar IS, Nadarajah K, Malik NAA, Kumar IS, Nadarajah K.. 2020. Elicitor and receptor molecules: orchestrators of plant defense and immunity. International Journal of Molecular Sciences 21, 963. PubMed PMC

Abrams JL, Verghese J, Gibney PA, Morano KA.. 2014. Hierarchical functional specificity of cytosolic heat shock protein 70 (Hsp70) nucleotide exchange factors in yeast. Journal of Biological Chemistry 289, 13155–13167. PubMed PMC

Akhtar SS, Mekureyaw MF, Pandey C, Roitsch T.. 2020. Role of cytokinins for interactions of plants with microbial pathogens and pest insects. Frontiers in Plant Science 10, 1777. PubMed PMC

Alfenas-Zerbini P, Maia IG, Fávaro RD, Cascardo JCM, Brommonschenkel SH, Zerbini FM.. 2009. Genome-wide analysis of differentially expressed genes during the early stages of tomato infection by a potyvirus. Molecular Plant-Microbe Interactions 22, 352–361. PubMed

Anelli T, Sitia R.. 2008. Protein quality control in the early secretory pathway. The EMBO Journal 27, 315–327. PubMed PMC

Aoki K, Kragler F, Xoconostle-Cazares B, Lucas WJ, Xoconostle-Cázares B, Lucas WJ.. 2002. A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proceedings of the National Academy of Sciences, USA 99, 16342–16347. PubMed PMC

Asea AAA,Calderwood SK, Kaur P., eds.2016. Heat shock proteins and plants. Cham: Springer International Publishing.

Ashraf M, Mao Q, Hong J, Shi L, Ran X, Liaquat F, Uzair M, Liang W, Fernie AR, Shi J.. 2021. HSP70-16 and VDAC3 jointly inhibit seed germination under cold stress in Arabidopsis. Plant, Cell & Environment 44, 3616–3627. PubMed

Bateman A, Martin MJ, O’Donovan C, et al. . 2017. UniProt: the universal protein knowledgebase. Nucleic Acids Research 45, D158–D169. PubMed PMC

Berka M, Greplová M, Saiz-Fernández I, Novák J, Luklová M, Zelená P, Tomšovský M, Brzobohatý B, Černý M.. 2020. Peptide-based identification of Phytophthora isolates and Phytophthora detection in planta. International Journal of Molecular Sciences 21, 1–17. PubMed PMC

Bernabò P, Viero G, Lencioni V.. 2020. A long noncoding RNA acts as a posttranscriptional regulator of heat shock protein (HSP70) synthesis in the cold hardy Diamesa tonsa under heat shock. PLoS One 15, e0227172. PubMed PMC

Borchiellini C, Boury-Esnault N, Vacelet J, Le Parco Y.. 1998. Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Molecular Biology and Evolution 15, 647–655. PubMed

Bracher A, Verghese J.. 2015. The nucleotide exchange factors of Hsp70 molecular chaperones. Frontiers in Molecular Biosciences 2, 10. PubMed PMC

Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SPP.. 2009. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host & Microbe 6, 457–469. PubMed PMC

Carvalho HH, Silva PA, Mendes GC, Brustolini OJB, Pimenta MR, Gouveia BC, Valente MAS, Ramos HJO, Soares-Ramos JRL, Fontes EPB.. 2014. The endoplasmic reticulum binding protein BiP displays dual function in modulating cell death events. Plant Physiology 164, 654–670. PubMed PMC

Cazalé A-C, Clément M, Chiarenza S, Roncato M-A, Pochon N, Creff A, Marin E, Leonhardt N, Noël LD.. 2009. Altered expression of cytosolic/nuclear HSC70-1 molecular chaperone affects development and abiotic stress tolerance in Arabidopsis thaliana. Journal of Experimental Botany 60, 2653–2664. PubMed

Cerna H, Černý M, Habánová H, Šafářová D, Abushamsiya K, Navrátil M, Brzobohatý B.. 2017. Proteomics offers insight to the mechanism behind Pisum sativum L. response to Pea seed-borne mosaic virus (PSbMV). Journal of Proteomics 153, 78–88. PubMed

Černý M, Jedelský PL, Novák J, Schlosser A, Brzobohatý B.. 2014. Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant, Cell & Environment 37, 1641–1655. PubMed

Černý M, Novák J, Habánová H, Cerna H, Brzobohatý B.. 2016. Role of the proteome in phytohormonal signaling. Biochimica et Biophysica Acta 1864, 1003–1015. PubMed

Černý M, Skalák J, Cerna H, Brzobohatý B.. 2013. Advances in purification and separation of posttranslationally modified proteins. Journal of Proteomics 92, 2–27. PubMed

Cha-Molstad H, Sung KS, Hwang J, et al. . 2015. Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through p62 binding. Nature Cell Biology 17, 917–929. PubMed PMC

Chen H, Cao Y, Li Y, Xia Z, Xie J, Carr JP, Wu B, Fan Z, Zhou T.. 2017. Identification of differentially regulated maize proteins conditioning Sugarcane mosaic virus systemic infection. New Phytologist 215, 1156–1172. PubMed

Chen T, Lv Y, Zhao T, Li N, Yang Y, Yu W, He X, Liu T, Zhang B.. 2013. Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS One 8, e80816. PubMed PMC

Chen X, Shi L, Chen Y, Zhu L, Zhang D, Xiao S, Aharoni A, Shi J, Xu J.. 2019. Arabidopsis HSP70-16 is required for flower opening under normal or mild heat stress temperatures. Plant, Cell & Environment 42, 1190–1204. PubMed

Clément M, Leonhardt N, Droillard M-JJ, et al. . 2011. The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiology 156, 1481–1492. PubMed PMC

Cloutier P, Coulombe B.. 2013. Regulation of molecular chaperones through post-translational modifications: decrypting the chaperone code. Biochimica et Biophysica Acta 1829, 443–454. PubMed PMC

Coelho AC, Pires R, Schütz G, Santa CC, Manadas B, Pinto PP, Schutz G, Santa CC, Manadas B, Pinto PP.. 2021. Disclosing proteins in the leaves of cork oak plants associated with the immune response to Phytophthora cinnamomi inoculation in the roots: a long-term proteomics approach. PLoS One 16, e0245148. PubMed PMC

Craig EA. 2018. Hsp70 at the membrane: driving protein translocation. BMC Biology 16, 11. PubMed PMC

Crampton BG, Hein I, Berger DK.. 2009. Salicylic acid confers resistance to a biotrophic rust pathogen, Puccinia substriata, in pearl millet (Pennisetum glaucum). Molecular Plant Pathology 10, 291–304. PubMed PMC

Eichmann R, Schäfer P.. 2012. The endoplasmic reticulum in plant immunity and cell death. Frontiers in Plant Science 3, 200. PubMed PMC

Espinoza C, Vega A, Medina C, Schlauch K, Cramer G, Arce-Johnson P.. 2007. Gene expression associated with compatible viral diseases in grapevine cultivars. Functional & Integrative Genomics 7, 95–110. PubMed

Fernández-Fernández MR, Gragera M, Ochoa-Ibarrola L, Quintana-Gallardo L, Valpuesta JM.. 2017. Hsp70—a master regulator in protein degradation. FEBS Letters 591, 2648–2660. PubMed

Gaguancela OA, Źuñiga LP, Arias AV, Halterman D, Flores FJ, Johansen IE, Wang A, Yamaji Y, Verchot J.. 2016. The IRE1/bZIP60 pathway and bax inhibitor 1 suppress systemic accumulation of potyviruses and potexviruses in Arabidopsis and Nicotiana benthamiana plants. Molecular Plant-Microbe Interactions 29, 750–766. PubMed

Góngora-Castillo E, Ibarra-Laclette E, Trejo-Saavedra DL, Rivera-Bustamante RF.. 2012. Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virology Journal 9, 295. PubMed PMC

Gorovits R, Moshe A, Ghanim M, Czosnek H.. 2013. Recruitment of the host plant heat shock protein 70 by Tomato yellow leaf curl virus coat protein is required for virus infection. PLoS One 8, e70280. PubMed PMC

Guo H, Zhang H, Wang G, Wang C, Wang Y, Liu X, Ji W.. 2021. Identification and expression analysis of heat-shock proteins in wheat infected with powdery mildew and stripe rust. The Plant Genome 14, e20092. PubMed

Gupta S, Bhar A, Chatterjee M, Ghosh A, Das S, Gupta V.. 2017. Transcriptomic dissection reveals wide spread differential expression in chickpea during early time points of Fusarium oxysporum f. sp. ciceri Race 1 attack. PLoS One 12, e0178164. PubMed PMC

Guy CL, Li Q-B.. 1998. The organization and evolution of the spinach stress 70 molecular chaperone gene family. The Plant Cell 10, 539–556. PubMed PMC

Hafrén A, Hofius D, Rönnholm G, Sonnewald U, Mäkinen K.. 2010. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. The Plant Cell 22, 523–535. PubMed PMC

Hayano-Saito Y, Hayashi K.. 2020. Stvb-i, a rice gene conferring durable resistance to Rice stripe virus, protects plant growth from heat stress. Frontiers in Plant Science 11, 519. PubMed PMC

Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH.. 2017. SUBA4: the interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Research 45, D1064–D1074. PubMed PMC

Huang L-H, Wang H-S, Kang L.. 2008. Different evolutionary lineages of large and small heat shock proteins in eukaryotes. Cell Research 18, 1074–1076. PubMed

Huang X, Hou L, Meng J, You H, Li Z, Gong Z, Yang S, Shi Y.. 2018. The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Molecular Plant 11, 970–982. PubMed

Hýsková V, Bělonožníková K, Čeřovská N, Ryšlavá H.. 2021a. HSP70 plays an ambiguous role during viral infections in plants. Biologia Plantarum65, 68–79.

Hýsková V, Bělonožníková K, Doričová V, Kavan D, Gillarová S, Henke S, Synková H, Ryšlavá H, Čeřovská N.. 2021b. Effects of heat treatment on metabolism of tobacco plants infected with Potato virus Y. Plant Biology 23, 131–141. PubMed

Jelenska J, van Hal JA, Greenberg JT.. 2010. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proceedings of the National Academy of Sciences, USA 107, 13177–13182. PubMed PMC

Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT.. 2007. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Current Biology 17, 499–508. PubMed PMC

Jing M, Guo B, Li H, et al. . 2016. A Phytophthora sojae effector suppresses endoplasmic reticulum stress-mediated immunity by stabilizing plant binding immunoglobulin proteins. Nature Communications 7, 11685. PubMed PMC

Jing M, Wang Y.. 2020. Plant pathogens utilize effectors to hijack the host endoplasmic reticulum as part of their infection strategy. Engineering 6, 500–504.

Jungkunz I, Link K, Vogel F, Voll LM, Sonnewald S, Sonnewald U.. 2011. AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. The Plant Journal 66, 983–995. PubMed

Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi R.. 2003. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Molecular Plant Pathology 4, 383–391. PubMed

Kim NH, Hwang BK.. 2015. Pepper heat shock protein 70a interacts with the type III effector AvrBsT and triggers plant cell death and immunity. Plant Physiology 167, 307–322. PubMed PMC

Kityk R, Kopp J, Mayer MP.. 2018. Molecular mechanism of J-domain-triggered ATP hydrolysis by Hsp70 chaperones. Molecular Cell 69, 227-237.e4. PubMed

Kityk R, Kopp J, Sinning I, Mayer MP.. 2012. Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Molecular Cell 48, 863–874. PubMed

Kityk R, Vogel M, Schlecht R, Bukau B, Mayer MP.. 2015. Pathways of allosteric regulation in Hsp70 chaperones. Nature Communications 6, 8308. PubMed PMC

Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF.. 2007. Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Planta 226, 1389–1409. PubMed

Kozeko L. 2021. Different roles of inducible and constitutive HSP70 and HSP90 in tolerance of Arabidopsis thaliana to high temperature and water deficit. Acta Physiologiae Plantarum 43, 58.

Krenz B, Windeisen V, Wege C, Jeske H, Kleinow T.. 2010. A plastid-targeted heat shock cognate 70 kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401, 6–17. PubMed

Krishnakumar V, Contrino S, Cheng CY, Belyaeva I, Ferlanti ES, Miller JR, Vaughn MW, Micklem G, Town CD, Chan AP.. 2017. Thalemine: a warehouse for Arabidopsis data integration and discovery. Plant & Cell Physiology 58, e4. PubMed

Latijnhouwers M, Xu X-MM, Møller SG.. 2010. Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232, 567–578. PubMed

Lee JH, Lee SE, Oh S, Seo E, Choi D.. 2018. HSP70s enhance a Phytophthora infestans effector-induced cell death via an MAPK cascade in Nicotiana benthamiana. Molecular Plant-Microbe Interactions 31, 356–362. PubMed

Lee SS, Lee DW, Lee Y, Mayer U, Stierhof Y-DD, Lee SS, Jürgens G, Hwang I, Jürgens G, Hwang I.. 2009. Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin–26S proteasome system in Arabidopsis. The Plant Cell 21, 3984–4001. PubMed PMC

Lescat L, Véron V, Mourot B, et al. . 2020. Chaperone-mediated autophagy in the light of evolution: insight from fish. Molecular Biology and Evolution 37, 2887–2899. PubMed

Li L, Nelson CJ, Trösch J, Castleden I, Huang S, Millar AH.. 2017. Protein degradation rate in Arabidopsis thaliana leaf growth and development. The Plant Cell 29, 207–228. PubMed PMC

Li Y, Kabbage M, Liu W, Dickman MB.. 2016. Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants. The Plant Cell 28, 233–247. PubMed PMC

Li Y, Williams B, Dickman M.. 2017. Arabidopsis B-cell lymphoma2 (Bcl-2)-associated athanogene 7 (BAG7)-mediated heat tolerance requires translocation, sumoylation and binding to WRKY29. New Phytologist 214, 695–705. PubMed

Liebrand TWH, Kombrink A, Zhang Z, Sklenar J, Jones AME, Robatzek S, Thomma BPHJ, Joosten MHAJ.. 2014. Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium. Molecular Plant Pathology 15, 109–117. PubMed PMC

Liebrand TWH, Smit P, Abd-El-Haliem A, et al. . 2012. Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiology 159, 1819–1833. PubMed PMC

Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M.. 2001. Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress and Chaperones 6, 201–208. PubMed PMC

Liu G-TT, Wang B-BB, Lecourieux D, et al. . 2021. Proteomic analysis of early-stage incompatible and compatible interactions between grapevine and P. viticola. Horticulture Research 8, 100. PubMed PMC

Lu Y, Yin M, Wang X, et al. . 2016. The unfolded protein response and programmed cell death are induced by expression of Garlic virus X p11 in Nicotiana benthamiana. Journal of General Virology 97, 1462–1468. PubMed

Lyu S, Gao L, Zhang R, Zhang C, Hou X.. 2020. Correlation analysis of expression profile and quantitative iTRAQ-LC-MS/MS proteomics reveals resistance mechanism against TuMV in Chinese cabbage (Brassica rapa ssp. pekinensis). Frontiers in Genetics 11, 963. PubMed PMC

Mambula SS, Stevenson MA, Ogawa K, Calderwood SK.. 2007. Mechanisms for Hsp70 secretion: crossing membranes without a leader. Methods 43, 168–175. PubMed PMC

Maruyama D, Endo T, Nishikawa S-i.. 2010. BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 107, 1684–1689. PubMed PMC

Maruyama D, Sugiyama T, Endo T, Nishikawa SI.. 2014. Multiple BiP genes of Arabidopsis thaliana are required for male gametogenesis and pollen competitiveness. Plant & Cell Physiology 55, 801–810. PubMed

Mergner J, Frejno M, List M, et al. . 2020. Mass-spectrometry-based draft of the Arabidopsis proteome. Nature 579, 409–414. PubMed

Mine A, Hyodo K, Tajima Y, Kusumanegara K, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T.. 2012. Differential roles of Hsp70 and Hsp90 in the assembly of the replicase complex of a positive-strand RNA plant virus. Journal of Virology 86, 12091–12104. PubMed PMC

Molitor A, Zajic D, Voll LM, Pons-Kühnemann J, Samans B, Kogel KH, Waller F.. 2011. Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica-mediated systemic induced resistance to powdery mildew. Molecular Plant-Microbe Interactions 24, 1427–1439. PubMed

Moon JY, Lee JH, Oh C-SS, Kang H-GG, Park JM.. 2016. Endoplasmic reticulum stress responses function in the HRT-mediated hypersensitive response in Nicotiana benthamiana. Molecular Plant Pathology 17, 1382–1397. PubMed PMC

Morgner N, Schmidt C, Beilsten-Edmands V, et al. . 2015. Hsp70 forms antiparallel dimers stabilized by post-translational modifications to position clients for transfer to Hsp90. Cell Reports 11, 759–769. PubMed PMC

Nagashima Y, Iwata Y, Ashida M, Mishiba KI, Koizumi N.. 2014. Exogenous salicylic acid activates two signaling arms of the unfolded protein response in Arabidopsis. Plant & Cell Physiology 55, 1772–1778. PubMed

Nakai M. 2018. New perspectives on chloroplast protein import. Plant & Cell Physiology 59, 1111–1119. PubMed

Nakashima A, Chen L, Thao NP, et al. . 2008. RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. The Plant Cell 20, 2265–2279. PubMed PMC

Naveed ZA, Ali GS.. 2018. Comparative transcriptome analysis between a resistant and a susceptible wild tomato accession in response to Phytophthora parasitica. International Journal of Molecular Sciences 19, 3735. PubMed PMC

Nekrasov V, Li J, Batoux M, et al. . 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. The EMBO Journal 28, 3428–3438. PubMed PMC

Nelson RS, Citovsky V.. 2005. Plant viruses. Invaders of cells and pirates of cellular pathways. Plant Physiology 138, 1809–1814. PubMed PMC

Nitika, Porter CM, Truman AW, Truttmann MC.. 2020. Post-translational modifications of Hsp70 family proteins: expanding the chaperone code. Journal of Biological Chemistry 295, 10689–10708. PubMed PMC

Noël LD, Cagna G, Stuttmann J, et al. . 2007. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. The Plant Cell 19, 4061–4076. PubMed PMC

Noh S-JJ, Kwon CS, Oh D-HH, Moon JS, Chung W-I.. 2003. Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311, 81–91. PubMed

Nürnberger T, Kemmerling B.. 2009. Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. Annual Plant Reviews 34, 16–47.

Omasits U, Ahrens CH, Müller S, Wollscheid B.. 2014. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30, 884–886. PubMed

Padmanabhan MS, Dinesh-Kumar SP.. 2010. All hands on deck—the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity. Molecular Plant-Microbe Interactions 23, 1368–1380. PubMed

Paiva ALSS, Oliveira JTAA, de Souza GA, Vasconcelos IM.. 2016. Label-free proteomic reveals that Cowpea severe mosaic virus transiently suppresses the host leaf protein accumulation during the compatible interaction with cowpea (Vigna unguiculata [L.] Walp.). Journal of Proteome Research 15, 4208–4220. PubMed

Palmblad M, Mills DJ, Bindschedler LV.. 2008. Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. Journal of Proteome Research 7, 780–785. PubMed

Pan X, Zhu B, Luo Y, Fu D.. 2013. Unraveling the protein network of tomato fruit in response to necrotrophic phytopathogenic Rhizopus nigricans. PLoS One 8, e73034. PubMed PMC

Park C-JJ, Bart R, Chern M, Canlas PE, Bai W, Ronald PC.. 2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One 5, e9262. PubMed PMC

Park C-JJ, Seo Y-SS.. 2015. Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathology Journal 31, 323–333. PubMed PMC

Park CJ, Song MY, Kim CY, Jeon JS, Ronald PC.. 2014. Rice BiP3 regulates immunity mediated by the PRRs XA3 and XA21 but not immunity mediated by the NB-LRR protein, Pi5. Biochemical and Biophysical Research Communications 448, 70–75. PubMed

Pogany J, Stork J, Li Z, Nagy PD.. 2008. In vitro assembly of the Tomato bushy stunt virus replicase requires the host heat shock protein 70. Proceedings of the National Academy of Sciences, USA 105, 19956–19961. PubMed PMC

Poór P, Czékus Z, Tari I, Ördög A.. 2019. The multifaceted roles of plant hormone salicylic acid in endoplasmic reticulum stress and unfolded protein response. International Journal of Molecular Sciences 20, 5842. PubMed PMC

Prator CA, Chooi KM, Jones D, Davy MW, MacDiarmid RM, Almeida RPPP.. 2020. Comparison of two different host plant genera responding to grapevine leafroll-associated virus 3 infection. Scientific Reports 10, 8505. PubMed PMC

Qi R, Sarbeng EB, Liu QQ, et al. . 2013. Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nature Structural & Molecular Biology 20, 900–907. PubMed PMC

Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P.. 2012. The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. The Plant Cell 24, 794–809. PubMed PMC

Ratheesh Kumar R, Nagarajan NS, Arunraj SP, Sinha D, Veedin Rajan VB, Esthaki VK, D’Silva P.. 2012. HSPIR: a manually annotated heat shock protein information resource. Bioinformatics 28, 2853–2855. PubMed PMC

Regente M, Pinedo M, San Clemente H, Balliau T, Jamet E, de la Canal L.. 2017. Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. Journal of Experimental Botany 68, 5485–5495. PubMed

Ritossa F. 1996. Discovery of the heat shock response. Cell Stress & Chaperones 1, 97. PubMed PMC

Rosenzweig R, Nillegoda NB, Mayer MP, Bukau B.. 2019. The Hsp70 chaperone network. Nature Reviews. Molecular Cell Biology 20, 665–680. PubMed

Rowarth NM, Dauphinee AN, Denbigh GL, Gunawardena AH.. 2020. Hsp70 plays a role in programmed cell death during the remodelling of leaves of the lace plant (Aponogeton madagascariensis). Journal of Experimental Botany 71, 907–918. PubMed

Rüdiger S, Germeroth L, Schneider-Mergener J, Bukau B, Rudiger S.. 1997. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. The EMBO Journal 16, 1501–1507. PubMed PMC

Saiz-Fernández I, Milenković I, Berka M, Černý M, Tomšovský M, Brzobohatý B, Kerchev P.. 2020. Integrated proteomic and metabolomic profiling of Phytophthora cinnamomi attack on sweet chestnut (Castanea sativa) reveals distinct molecular reprogramming proximal to the infection site and away from it. International Journal of Molecular Sciences 21, 8525. PubMed PMC

Sarkar NK, Kundnani P, Grover A.. 2013. Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress and Chaperones 18, 427–437. PubMed PMC

Schleiff E, Becker T.. 2011. Common ground for protein translocation: access control for mitochondria and chloroplasts. Nature Reviews. Molecular Cell Biology 12, 48–59. PubMed

Sharma Poudel R, Richards J, Shrestha S, Solanki S, Brueggeman R.. 2019. Transcriptome-wide association study identifies putative elicitors/suppressor of Puccinia graminis f. sp. tritici that modulate barley rpg4-mediated stem rust resistance. BMC Genomics 20, 985. PubMed PMC

Shirasu K. 2009. The HSP90–SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology 60, 139–164. PubMed

Singh P, Song Q-Q, Singh R, Li H-B, Solanki M, Malviya M, Verma K, Yang L-T, Li Y-R.. 2019. Proteomic analysis of the resistance mechanisms in sugarcane during Sporisorium scitamineum infection. International Journal of Molecular Sciences 20, 569. PubMed PMC

Song T, Ma Z, Shen D, Li Q, Li W, Su L, Ye T, Zhang M, Wang Y, Dou D.. 2015. An oomycete CRN effector reprograms expression of plant HSP genes by targeting their promoters. PLoS Pathogens 11, e1005348. PubMed PMC

Sousa R, Lafer EM.. 2019. The physics of entropic pulling: a novel model for the Hsp70 motor mechanism. International Journal of Molecular Sciences 20, 2334. PubMed PMC

Strasser R. 2018. Protein quality control in the endoplasmic reticulum of plants. Annual Review of Plant Biology 69, 147–172. PubMed PMC

Su PH, Li HM.. 2008. Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiology 146, 1231–1241. PubMed PMC

Su P-HH, Li HM.. 2010. Stromal hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. The Plant Cell 22, 1516–1531. PubMed PMC

Sun J-LL, Li J-YY, Wang M-JJ, Song Z-TT, Liu J-XX.. 2021. Protein quality control in plant organelles: current progress and future perspectives. Molecular Plant 14, 95–114. PubMed

Sung DY, Guy CL.. 2003. Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiology 132, 979–987. PubMed PMC

Szajko K, Plich J, Przetakiewicz J, Sołtys-Kalina D, Marczewski W.. 2020. Comparative proteomic analysis of resistant and susceptible potato cultivars during Synchytrium endobioticum infestation. Planta 251, 4. PubMed

Takakuwa JE, Nitika Knighton LE, Truman AW.. 2019. Oligomerization of Hsp70: current perspectives on regulation and function. Frontiers in Molecular Biosciences 6, 81. PubMed PMC

Thao NP, Chen L, Nakashima A, Hara SI, Umemura K, Takahashi A, Shirasu K, Kawasaki T, Shimamoto K.. 2007. RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. The Plant Cell 19, 4035–4045. PubMed PMC

Tichá T, Samakovli D, Kuchařová A, Vavrdová T, Šamaj J.. 2020. Multifaceted roles of HEAT SHOCK PROTEIN 90 molecular chaperones in plant development. Journal of Experimental Botany 71, 3966–3985. PubMed

Tissiéres A, Mitchell HK, Tracy UM.. 1974. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. Journal of Molecular Biology 84, 389–398. PubMed

Ul Haq S, Khan A, Ali M, Khattak AM, Gai WX, Zhang HX, Wei AM, Gong ZH.. 2019. Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. International Journal of Molecular Sciences 20, 5321. PubMed PMC

Usman MG, Rafii MY, Martini MY, Yusuff OA, Ismail MR, Miah G.. 2017. Molecular analysis of Hsp70 mechanisms in plants and their function in response to stress. Biotechnology and Genetic Engineering Reviews 33, 26–39. PubMed

van der Burgh A M, Joosten MHAJ.. 2019. Plant immunity: thinking outside and inside the box. Trends in Plant Science 24, 587–601. PubMed

van Wijk KJ, LeppertT, Sun Q, Boguraev SS, Sun Z, Mendoza L, Deutsch EW.. 2021. The Arabidopsis thaliana PeptideAtlas; harnessing world-wide proteomics data for a comprehensive community proteomics resource. bioRxiv 2021, 05.03.442425. [Preprint]. PubMed PMC

Varela ALN, Komatsu S, Wang X, Silva RGG, Souza PFN, Lobo AKM, Vasconcelos IM, Silveira JAG, Oliveira JTA.. 2017. Gel-free/label-free proteomic, photosynthetic, and biochemical analysis of cowpea (Vigna unguiculata [L.] Walp.) resistance against Cowpea severe mosaic virus (CPSMV). Journal of Proteomics 163, 76–91. PubMed

Verma AK, Tamadaddi C, Tak Y, Lal SS, Cole SJ, Hines JK, Sahi C.. 2019. The expanding world of plant J-domain proteins. Critical Reviews in Plant Sciences 38, 382–400. PubMed PMC

Vitale A, Rocco M, Arena S, et al. . 2014. Tomato susceptibility to Fusarium crown and root rot: effect of grafting combination and proteomic analysis of tolerance expression in the rootstock. Plant Physiology and Biochemistry 83, 207–216. PubMed

Wang D, Weaver ND, Kesarwani M, Dong X.. 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308, 1036–1040. PubMed

Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M.. 2016. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nature Communications 7, 10269. PubMed PMC

Wang W, Vinocur B, Shoseyov O, Altman A.. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9, 244–252. PubMed

Wang Y, Gibney PA, West JD, Morano KA.. 2012. The yeast Hsp70 Ssa1 is a sensor for activation of the heat shock response by thiol-reactive compounds. Molecular Biology of the Cell 23, 3290–3298. PubMed PMC

Waterhouse A, Bertoni M, Bienert S, et al. . 2018. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Research 46, W296–W303. PubMed PMC

Waterhouse AM, Procter JB, Martin DMAA, Clamp M, Barton GJ.. 2009. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191. PubMed PMC

Waters ER, Rioflorido I.. 2007. Evolutionary analysis of the small heat shock proteins in five complete algal genomes. Journal of Molecular Evolution 65, 162–174. PubMed

Waters ER, Vierling E.. 2020. Plant small heat shock proteins—evolutionary and functional diversity. New Phytologist 227, 24–37. PubMed

Wei S-SS, Niu W-TT, Zhai X-TT, et al. . 2019. Arabidopsis mtHSC70-1 plays important roles in the establishment of COX-dependent respiration and redox homeostasis. Journal of Experimental Botany 70, 5575–5590. PubMed

Weigel D, Mott R.. 2009. The 1001 Genomes Project for Arabidopsis thaliana. Genome Biology 10, 107. PubMed PMC

Willems P, Horne A, Van Parys T, Goormachtig S, De Smet I, Botzki A, Van Breusegem F, Gevaert K.. 2019. The Plant PTM Viewer, a central resource for exploring plant protein modifications. The Plant Journal 99, 752–762. PubMed

Williams B, Kabbage M, Britt R, Dickman MB.. 2010. AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proceedings of the National Academy of Sciences, USA 107, 6088–6093. PubMed PMC

Wu X, Yan J, Wu Y, Zhang H, Mo S, Xu X, Zhou F, Ding H.. 2019. Proteomic analysis by iTRAQ-PRM provides integrated insight into mechanisms of resistance in pepper to Bemisia tabaci (Gennadius). BMC Plant Biology 19, 270. PubMed PMC

Xu G, Li S, Xie K, Zhang Q, Wang Y, Tang Y, Liu D, Hong Y, He C, Liu Y.. 2012. Plant ERD2-like proteins function as endoplasmic reticulum luminal protein receptors and participate in programmed cell death during innate immunity. The Plant Journal 72, 57–69. PubMed

Xu L , Nitika Hasin N, Cuskelly DD, Wolfgeher D, Doyle S, Moynagh P, Perrett S, Jones GW, Truman AW.. 2019. Rapid deacetylation of yeast Hsp70 mediates the cellular response to heat stress. Scientific Reports 9, 16260. PubMed PMC

Yang J, Zhang F, Cai N-JJ, Wu N, Chen X, Li J, Meng X-FF, Zhu T-QQ, Chen J-PP, Zhang H-MM.. 2017. A furoviral replicase recruits host HSP70 to membranes for viral RNA replication. Scientific Reports 7, 45590. PubMed PMC

Ye C, Dickman MB, Whitham SA, Payton M, Verchot J.. 2011. The unfolded protein response is triggered by a plant viral movement protein. Plant Physiology 156, 741–755. PubMed PMC

Zemanovic S, Ivanov MV., Ivanova LV., et al. . 2018. Dynamic phosphorylation of the C terminus of Hsp70 regulates the mitochondrial import of SOD2 and redox balance. Cell Reports 25, 2605–2616.e7. PubMed PMC

Zhang C, Tian Y, Cong P.. 2015. Proteome analysis of pathogen-responsive proteins from apple leaves induced by the alternaria blotch Alternaria alternata. PLoS One 10, e0122233. PubMed PMC

Zhang H, Zhang F, Yu Y, Feng L, Jia J, Liu B, Li B, Guo H, Zhai J.. 2020. A comprehensive online database for exploring ~20,000 public Arabidopsis RNA-Seq libraries. Molecular Plant 13, 1231–1233. PubMed

Zhang X-C, Millet YA, Cheng Z, Bush J, Ausubel FM.. 2015. Jasmonate signalling in Arabidopsis involves SGT1b–HSP70–HSP90 chaperone complexes. Nature Plants 1, 15049. PubMed PMC

Zhang Y, Xia G, Zhu Q.. 2021. Conserved and unique roles of chaperone-dependent E3 ubiquitin ligase CHIP in plants. Frontiers in Plant Science 12, 699756. PubMed PMC

Zhang Z, Shrestha J, Tateda C, Greenberg JT.. 2014. Salicylic acid signaling controls the maturation and localization of the Arabidopsis defense protein ACCELERATED CELL DEATH6. Molecular Plant 7, 1365–1383. PubMed PMC

Zhou Y, Yang K, Cheng M, et al. . 2021. Double-faced role of Bcl-2-associated athanogene 7 in plant–Phytophthora interaction. Journal of Experimental Botany 72, 5751–5765. PubMed

Zuiderweg ERP, Hightower LE, Gestwicki JE.. 2017. The remarkable multivalency of the Hsp70 chaperones. Cell Stress and Chaperones 22, 173–189. PubMed PMC

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