Skip to main content
SpringerLink
Log in

The Role of HSP90 Chaperones in Stability and Plasticity of Ontogenesis of Plants under Normal and Stressful Conditions (Arabidopsis thaliana)

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

The functions of HSP90 chaperones in the protein-folding system and regulation of specific substrates affecting multiple signal pathways and cellular processes were considered. The triple role of HSP90 in stress was described: binding damaged proteins and directing them for refolding or degradation, regulation of the heat-shock gene induction, and alteration in the gene expression program. Based on the results of studies of the model species Arabidopsis thaliana, the role of HSP90 in growth maintenance and morphogenesis stability, developmental plasticity, and mechanisms of stress tolerance in plants was shown. A model for the interaction of the HSP90 functions under normal and stressful conditions is presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Picard, D., Heat-shock protein 90, a chaperone for folding and regulation, Cell. Mol. Life Sci., 2002, vol. 59, no. 10, pp. 1640–1648. https://doi.org/10.1007/PL00012491

    Article  CAS  PubMed  Google Scholar 

  2. Nollen, E.A.A. and Morimoto, R.I., Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins, J. Cell Sci., 2002, vol. 115, no. 14, pp. 2809–2816.

    CAS  PubMed  Google Scholar 

  3. Pearl, L.H. and Prodromou, C., Structure and in vivo function of Hsp90, Curr. Opin. Struct. Biol., 2000, vol. 10, no. 1, pp. 46–51. https://doi.org/10.1016/S0959-440X(99)00047-0

    Article  CAS  PubMed  Google Scholar 

  4. Zhao, R., Davey, M., Hsu, Y.C., Kaplanek, P., Tong, A., Parsons, A.B., Krogan, N., Cagney, G., Mai, D., Greenblatt, J., Boone, C., Emili, A., and Houry, W.A., Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the Hsp90 chaperone, Cell, 2005, vol. 120, no. 5, pp. 715–727. https://doi.org/10.1016/j.cell.2004.12.024

    Article  CAS  PubMed  Google Scholar 

  5. Kozeko, L.Ye., Heat shock proteins 90 kDa: diversity, structure, functions, Tsitologyia, 2010, vol. 52, no. 11, pp. 3–20.

    Google Scholar 

  6. Taipale, M., Jarosz, D., and Lindquist, S., HSP90 at the hub of protein homeostasis: emerging mechanistic insights, Nat. Rev. Mol. Cell Biol. 2010, vol. 11, no. 7, pp. 515–528. https://doi.org/10.1038/nrm2918

    Article  CAS  PubMed  Google Scholar 

  7. Zou, J., Guo, Y., Guettouche, T., Smith, D.F., and Voellmy, R., Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1, Cell, 1998, vol. 94, no. 4, pp. 471–480. https://doi.org/10.1016/S0092-8674(00)81588-3

    Article  CAS  PubMed  Google Scholar 

  8. Morimoto, R.I., Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators, Gen. Dev., 1998, vol. 12, no. 24, pp. 3788–3796. https://doi.org/10.1101/gad.12.24.3788

    Article  CAS  Google Scholar 

  9. Rutherford, S.L. and Lindquist, S., Hsp90 as a capacitor for morphological evolution, Nature, 1998, vol. 396, no. 6709, pp. 336–342. https://doi.org/10.1038/24550

    Article  CAS  PubMed  Google Scholar 

  10. Queitsch, C., Sangster, T.A., and Lindquist, S., Hsp90 as a capacitor of phenotypic variation, Nature, 2002, vol. 417, no. 6889, pp. 618–624. https://doi.org/10.1038/nature749

    Article  CAS  PubMed  Google Scholar 

  11. Samakovli, D., Thanou, A., Valmas, C., and Hatzopoulos, P., Hsp90 canalizes developmental perturbation, J. Exp. Bot., 2007, vol. 58, no. 13, pp. 3515–3524. https://doi.org/10.1093/jxb/erm191

    Article  CAS  Google Scholar 

  12. Sangster, T.A., Bahrami, A., Wilczek, A., Watanabe, E., Schellenberg, K., McLellan, C., Kelley, A., Kong, S.W., Queitsch, C., and Lindquist, S., Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels, PLoS One, 2007, no. 7, e648. https://doi.org/10.1371/journal.pone.0000648

  13. Jarosz, D.F. and Lindquist, S., Hsp90 and environmental stress transform the adaptive value of natural genetic variation, Science, 2010, vol. 330, no. 6012, pp. 1820–1824. https://doi.org/10.1126/science.1195487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Sangster, T.A., Lindquist, S., and Queitsch, C., Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance, BioEssays, 2004, vol. 26, no. 4, pp. 348–362. https://doi.org/10.1002/bies.20020

    Article  CAS  PubMed  Google Scholar 

  15. Rutherford, S., Hirate, Y., and Swala, B.J., The Hsp90 capacitor, developmental remodeling, and evolution: The robustness of gene networks and the curious evolvability of metamorphosis, Crit. Rev. Biochem. Mol. Biol., 2007, vol. 42, no. 5, pp. 355–372. https://doi.org/10.1080/10409230701597782

    Article  CAS  PubMed  Google Scholar 

  16. Krishna, P. and Gloor, G., The Hsp90 family of proteins in Arabidopsis thaliana, Cell Stres. Chaper., 2001, vol. 6, no. 3, pp. 238–246. doi 1379/1466-1268(2001)006<0238:THFOPI>2.0.CO;2

  17. Yamada, K., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I., and Nishimura, M., Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana, J. Biol. Chem., 2007, vol. 282, no. 52, pp. 37794–37804. https://doi.org/10.1074/jbc.M707168200

    Article  CAS  PubMed  Google Scholar 

  18. Cha, J.Y., Ahn, G., Kim, J.Y., Kang, S.B., Kim, M.R., Su’udi, M., Kim, W.Y., and Son, D., Structural and functional differences of cytosolic 90-kDa heat-shock proteins (Hsp90s) in Arabidopsis thaliana, Plant Physiol. Biochem., 2013, vol. 70, pp. 368–373. https://doi.org/10.1016/j.plaphy.2013.05.039

    Article  CAS  PubMed  Google Scholar 

  19. Karagoz, G.E. and Rudiger, S.G.D., Hsp90 interaction with clients, Trend. Biochem. Sci. 2015, vol. 40, no. 2, pp. 117–125. https://doi.org/10.1016/j.tibs.2014.12.002

    Article  CAS  PubMed  Google Scholar 

  20. Imai, J., Maruya, M., Yashiroda, H., Yahara, I., and Tanaka, K., The molecular chaperone Hsp90 plays a role in the assembly and maintenance of the 26S proteasome, EMBO J., 2003, vol. 22, no. 14, pp. 3557–3567. https://doi.org/10.1093/emboj/cdg349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Park, S.J., Suetsugu, S., and Takenawa, T., Interaction of Hsp90 to N-WASP leads to activation and protection from proteasome-dependent degradation, EMBO J., 2005, vol. 24, no. 8, pp. 1557–1570. https://doi.org/10.1038/sj.emboj.7600586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Holt, S.E., Aisner, D.L., Baur, J., Tesmer, V.M., Dy, M., Ouellette, M., Trager, J.B., Morin, G.B., Toft, D.O., Shay, J.W., Wright, W.E., and White, M.A., Functional requirement of p23 and Hsp90 in telomerase complexes, Gen. Dev., 1999, vol. 13, no. 7, pp. 817–826. https://doi.org/10.1101/gad.13.7.817

    Article  CAS  Google Scholar 

  23. Makhnevych, T. and Houry, W.A., The role of Hsp90 in protein complex assembly, Biochim. Biophys. Acta, 2012, vol. 1823, no. 3, pp. 674–682. https://doi.org/10.1016/j.bbamcr.2011.09.001

    Article  CAS  PubMed  Google Scholar 

  24. Kim, T.S., Jang, C.Y., Kim, H.D., Lee, J.Y., Ahn, B.Y., and Kim, J., Interaction of Hsp90 with ribosomal proteins protects from ubiquitination and proteasome-dependent degradation, Mol. Biol. Cell., 2006, vol. 17, no. 2, pp. 824–833. https://doi.org/10.1091/mbc.e05-08-0713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sawarkar, R., Sievers, C., and Paro, R., HSP90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli, Cell, 2012, vol. 149, no. 4, pp. 807–818. https://doi.org/10.1016/j.cell.2012.02.061

    Article  CAS  PubMed  Google Scholar 

  26. Uversky, V.N., Oldfield, C.J., and Dunker, A.K., Showing your ID: Intrinsic disorder as an ID for recognition, regulation and cell signaling, J. Mol. Rec., 2005, vol. 18, no. 5, pp. 343–384. https://doi.org/10.1002/jmr.747

    Article  CAS  Google Scholar 

  27. Hahn, A., Bublak, D., Schleiff, E., and Scharf, K.D., Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato, Plant Cell, 2011, vol. 23, no. 2, pp. 741–755. https://doi.org/10.1105/tpc.110.076018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Scharf, K.D., Berberich, T., Ebersberger, I., and Nover, L., The plant heat stress transcription factor (Hsf) family: structure, function and evolution, Biochim. Biophis. Acta, 2012, vol. 1819, no. 2, pp. 104–119. https://doi.org/10.1016/j.bbagrm.2011.10.002

    Article  CAS  Google Scholar 

  29. Liu, H.C., Liao, H.T., and 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, vol. 34, no. 5, pp. 738–751. https://doi.org/10.1111/j.1365-3040.2011.02278.x

    Article  CAS  Google Scholar 

  30. Charng, Y., Liu, H., Liu, N., Chi, W., Wang, C., Chang, S., and Wang, T., A heat-inducible transcription factor, HsfA2, is required for extension of acquire thermotolerance in Arabidopsis, Plant Physiol., 2007, vol. 143, no. 1, pp. 251–262. https://doi.org/10.1104/pp.106.091322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ogawa, D., Yamaguchi, K., and Nishiuchi, T., High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased thermotolerance but also salt/osmotic stress tolerance and enhanced callus growth, J. Exp. Bot., 2007, vol. 58, no. 12, pp. 3373–3383. https://doi.org/10.1093/jxb/erm184

    Article  CAS  PubMed  Google Scholar 

  32. Meiri, D. and Breiman, A., Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs, Plant J., 2009, vol. 59, no. 3, pp. 387–399. https://doi.org/10.1111/j.1365-313X.2009.03878.x

    Article  CAS  PubMed  Google Scholar 

  33. Meiri, D., Tazat, K., Cohen-Peer, R., Farchi-Pisanty, O., Aviezer-Hagai, K., Avni, A., and Breiman, A., Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance, Plant Mol. Biol., 2010, vol. 72, no. 1–2, pp. 191–203. https://doi.org/10.1007/s11103-009-9561-3

    Article  CAS  PubMed  Google Scholar 

  34. Scharf, K.D., Heider, H., Höhfeld, I., Lyck, R., Schmidt, E., and Nover, L., The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules, Mol. Cell. Biol., 1998, vol. 18, no. 4, pp. 2240–2251. https://doi.org/10.1128/MCB.18.4.2240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kim, S.H., Lee, J.H., Seo, K.I., Ryu, B., Sung, Y., Chung, T., Deng, X.W., and Lee, J.H., Characterization of a novel DWD protein that participates in heat stress response in Arabidopsis, Mol. Cells, 2014, vol. 37, no. 11, pp. 833–840. https://doi.org/10.14348/molcells.2014.0224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Samakovli, D., Margaritopoulou, T., Prassinos, C., Milioni, D., and Hatzopoulos, P., Brassinosteroid nuclear signaling recruits HSP90 activity, New Phytol., 2014, vol. 203, no. 3, pp. 743–757. https://doi.org/10.1111/nph.12843

    Article  CAS  PubMed  Google Scholar 

  37. Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J., BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation, Cell, 2002, vol. 109, no. 2, pp. 181–191. https://doi.org/10.1016/S0092-8674(02)00721-3

    Article  CAS  PubMed  Google Scholar 

  38. Lachowiec, J., Lemus, T., Thomas, J.H., Murphy, P.J.M., Nemhauser, J.L., and Queitsch, C., The protein chaperone HSP90 can facilitate the divergence of gene duplicates, Genetics, 2013, vol. 193, no. 4, pp. 1269–1277. https://doi.org/10.1534/genetics.112.148098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Shigeta, T., Zaizen, Y., Asami, T., Yoshida, S., Nakamura, Y., Okamoto, S., Matsuo, T., and Sugimoto, Y., Molecular evidence of the involvement of heat shock protein 90 in brassinosteroid signaling in Arabidopsis T87 cultured cells, Plant Cell Rep., 2014, vol. 33, no. 3, pp. 499–510. https://doi.org/10.1007/s00299-013-1550-y

    Article  CAS  PubMed  Google Scholar 

  40. Kim, T.S., Kim, W.Y., Fujiwara, S., Kim, J., Cha, J.Y., Park, J.H., Lee, S.Y., and Somers, D.E., HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no, 40, pp. 16843–16848. https://doi.org/10.1073/pnas.1110406108

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wang, R., Zhang, Y., Kieffer, M., Yu, H., Kepinski, S., and Estelle, M., HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1, Nat. Commun., 2016, vol. 7, p. 10269. doi .https://doi.org/10.1038/ncomms10269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Watanabe, E., Mano, S., Nomoto, M., Tada, Y., Hara-Nishimura, I., Nishimura, M., and Yamada, K., HSP90 stabilizes auxin-responsive phenotypes by masking a mutation in the auxin receptor TIR1, Plant Cell Physiol., 2016, vol. 57, no. 11, pp. 2245–2254. https://doi.org/10.1093/pcp/pcw170

    Article  CAS  PubMed  Google Scholar 

  43. Watanabe, E., Mano, S., Hara-Nishimura, I., Nishimura, M., and Yamada, K., HSP90 stabilizes auxin receptor TIR1 and ensures plasticity of auxin responses, Plant Signal. Behav., 2017, vol. 12, no. 5, e1311439. https://doi.org/10.1080/15592324.2017.1311439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Zhang, X.C., Millet, Y.A., Cheng, Z., Bush, J., and Ausubel, F.M., Jasmonate signalling in Arabidopsis involves SGT1b–HSP70–HSP90 chaperone complexes, Nat. Plants, 2015, vol. 1, 15049. https://doi.org/10.1038/nplants.2015.49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Song, Y.H., Estrada, D.A., Johnsonc, R.S., Kima, S.K., Leed, S.Y., MacCossc, M.J., and Imaizumia, T., Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering, Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, no. 49, pp. 17672–17677. https://doi.org/10.1073/pnas.1415375111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Smith, M.R., Willmann, M.R., Wu, G., Berardini, T.Z., Moller, B., Weijers, D., and Poethig, R.S., Cyclophilin 40 is required for microRNA activity in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 13, pp. 5424–5429. https://doi.org/10.1073/pnas.0812729106

    Article  PubMed  PubMed Central  Google Scholar 

  47. Iki, T., Yoshikawa, M., Nishikiori, M., Jaudal, M.C., Matsumoto-Yokoyama, E., Mitsuhara, I., Meshi, T., and Ishikawa, M., In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90, Mol. Cell., 2010, vol. 39, no. 2, pp. 282–291. https://doi.org/10.1016/j.molcel.2010.05.014

    Article  CAS  PubMed  Google Scholar 

  48. Earley, K.W. and Poethig, R.S., Binding of the cyclophilin 40 ortholog SQUINT to Hsp90 protein is required for SQUINT function in Arabidopsis, J. Biol. Chem., 2011, vol. 286, no. 44, pp. 38184–38189. https://doi.org/10.1074/jbc.M111.290130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chang, I.F., Curran, A., Woolsey, R., Quilici, D., Cushman, J., Mittler, R., Harmon, A., and Harper, J., Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana, Proteomics, 2009, vol. 9, no, 11, pp. 2967–2985. https://doi.org/10.1002/pmic.200800445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Swatek, K.N., Graham, K., Agrawal, G.K., and Thelen, J.J., The 14-3-3 isoforms chi and epsilon differentially bind client proteins from developing Arabidopsis seed, J. Prot. Res., 2011, vol. 10, no. 9, pp. 4076–4087. https://doi.org/10.1021/pr200263m

    Article  CAS  Google Scholar 

  51. Schweiger, R., Soll, J., Jung, K., Heermann, R., and Schwenkert, S., Quantification of interaction strengths between chaperones and tetratricopeptide repeat domain containing membrane proteins, J. Biol. Chem., 2013, vol. 288, no. 42, pp. 30614–30625. https://doi.org/10.1074/jbc.M113.493015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Inoue, H., Li, M., and Schnell, D.J., An essential role for chloroplast heat shock protein 90 (Hsp90C) in protein import into chloroplasts, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 8, pp. 3173–3178. https://doi.org/10.1073/pnas.1219229110

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kovacheva, S., Bédard, J., Patel, R., Twell, D., Ríos, G., Koncz, C., and Jarvis, P., In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import, Plant J., 2005, vol. 41, no. 3, pp. 412–428. https://doi.org/10.1111/j.1365-313X.2004.02307.x

    Article  CAS  PubMed  Google Scholar 

  54. Heide, H., Nordhues, A., Drepper, F., Nick, S., Schulz-Raffelt, M., Haehnel, W., and Schroda, M., Application of quantitative immunoprecipitation combined with knockdown and cross-linking to Chlamydomonas reveals the presence of vesicle-inducing protein in plastids 1 in a common complex with chloroplast HSP90C, Proteomics, 2009, vol. 9, no. 11, pp. 3079–3089. https://doi.org/10.1002/pmic.200800872

    Article  CAS  PubMed  Google Scholar 

  55. Feng, J., Fan, P., Jiang, P., Lv, S., Chen, X., and Li, Y., Chloroplast-targeted Hsp90 plays essential roles in plastid development and embryogenesis in Arabidopsis possibly linking with VIPP1, Physiol. Plant, 2014, vol. 150, no. 2, pp. 292–307. https://doi.org/10.1111/ppl.12083

    Article  CAS  PubMed  Google Scholar 

  56. Ishiguro, S., Watanabe, Y., Ito, N., Nonaka, H., Takeda, N., Sakai, T., Kanaya, H., and Okada, K., SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins, EMBO J., 2002, vol. 21, no. 5, pp. 898–908. https://doi.org/10.1093/emboj/21.5.898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Fujiwara, M., Uemura, T., Ebine, K., Nishimori, Y., Ueda, T., Nakano, A., Sato, M.H., and Fukao, Y., Interactomics of Qa-SNARE in Arabidopsis thaliana, Plant Cell Physiol., 2014, vol. 55, no 4, pp. 781–789. https://doi.org/10.1093/pcp/pcu038

    Article  CAS  PubMed  Google Scholar 

  58. Chong L.P., Wang Y., Gad N., Anderson N., Shah B., Zhao R. A highly charged region in the middle domain of plant endoplasmic reticulum (ER)-localized heat-shock protein 90 is required for resistance to tunicamycin or high calcium-induced ER stresses, J. Exp. Bot., 2015, vol. 66, no. 1, pp. 113–124. https://doi.org/10.1093/jxb/eru403

    Article  CAS  PubMed  Google Scholar 

  59. Carland, F.M., Fujioka, S., Takatsuto, S., Yoshida, S., and Nelson, T., The identification of CVP1 reveals a role for sterols in vascular patterning, Plant Cell, 2002, vol. 14, no. 9, pp. 2045–2058. https://doi.org/10.1105/tpc.003939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Hubert, D.A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K., and Dangl, J.L., Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein, EMBO J., 2003, vol. 22, no. 21, pp. 5679–5689. https://doi.org/10.1093/emboj/cdg547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Takahashi, A., Casais, C., Ichimura, K., and Shirasu, K., HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, no. 20, pp. 11777–11782. https://doi.org/10.1073/pnas.2033934100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lu, R., Malcuit, I., Moffett, P., Ruiz, M.T., Peart, J., Wu, A.J., Rathjen, J.P., Bendahmane, A., Day, L., and Baulcombe, D.C., High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance, EMBO J., 2003, vol. 22, no. 21, pp. 5690–5699. https://doi.org/10.1093/emboj/cdg546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S., and Dinesh-Kumar, S.P., Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants, J. Biol. Chem., 2004, vol. 279, no. 3, pp. 2101–2108. https://doi.org/10.1074/jbc.M310029200

    Article  CAS  PubMed  Google Scholar 

  64. Bieri, S., Mauch, S., Shen, Q.H., Peart, J., Devoto, A., Casais, C., Ceron, F., Schulze, S., Steinbiss, H.H., Shirasu, K., and Schulze-Lefert, P., RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance, Plant Cell, 2004, vol. 16, no. 12, pp. 3480–3495. https://doi.org/10.1105/tpc.104.026682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Holt III, B.F., Belkhadir, Y., and Dangl, J.L., Antagonistic control of disease resistance protein stability in the plant immune system, Science, 2005, vol. 309, no. 5736, pp. 929–932. https://doi.org/10.1126/science.1109977

    Article  CAS  PubMed  Google Scholar 

  66. Chen, L., Hamada, S., Fujiwara, M., Zhu, T., Thao, N.P., Wong, H.L., Krishna, P., Ueda, T., Kaku, H., Shibuya, N., Kawasaki, T., and Shimamoto, K., The Hop/Sti1–Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity, Cell Host Microbe, 2010, vol. 7, no. 3, pp. 185–196. https://doi.org/10.1016/j.chom.2010.02.008

    Article  CAS  PubMed  Google Scholar 

  67. Miwa, H., Kinoshita, A., Fukuda, H., and Sawa, S., Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem, J. Plant Res., 2009, vol. 122, no. 1, pp. 31–39. https://doi.org/10.1007/s10265-008-0207-3

    Article  CAS  PubMed  Google Scholar 

  68. You, Y., Sawikowska, A., Neumann, M., Posé, D., Capovilla, D., Langenecker, T., Neher, R.A., Krajewski, P., and Schmid, M., Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering, Nat. Commun., 2017, vol. 8, p. 15120. https://doi.org/10.1038/ncomms15120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sun, B. and Ito, T., Regulation of floral stem cell termination in Arabidopsis, Front. Plant Sci., 2015, vol. 6, p. 17. https://doi.org/10.3389/fpls.2015.00017

    Article  PubMed  PubMed Central  Google Scholar 

  70. Clouse, S.D., Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development, Plant Cell, 2011, vol. 23, no. 4, pp. 1219–1230. https://doi.org/10.1105/tpc.111.084475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kozeko, L.E., Phenotypic variability of Arabidopsis thaliana seedlings as a result of inhibition of Hsp90 chaperones, Cytol. Genet., 2013, vol. 47, no. 2, pp. 75–87. https://doi.org/10.3103/S0095452713020072

    Article  Google Scholar 

  72. Kozeko, L.Ye., Influence of radicicol, an inhibitor of HSP90 chaperons, on growth of Arabidopsis thaliana after gamma-irradiation of seeds, Bull. Kharkiv Natl. Agrar. Univ. Ser. Biol., 2015, vol. 34, no. 1, pp. 14–21.

  73. Craig, A., Ewan, R., Mesmar, J., Gudipati, V., and Sadanandom, A., E3 ubiquitin ligases and plant innate immunity, J. Exp. Bot., 2009, vol. 60, no. 4, pp. 1123–1132. https://doi.org/10.1093/jxb/erp059

    Article  CAS  PubMed  Google Scholar 

  74. Kadota, Y., Shirasu, K., and Guerois, R., NLR sensors meet at the SGT1-HSP90 crossroad, Trends Biochem. Sci., 2010, vol. 35, no. 4, pp. 199–207. https://doi.org/10.1016/j.tibs.2009.12.005

    Article  CAS  PubMed  Google Scholar 

  75. Waddington, C.H., Canalization of development and the inheritance of acquired characters, Nature, 1942, vol. 150, no. 3811, pp. 563–565. https://doi.org/10.1038/150563a0

    Article  Google Scholar 

  76. Gärtner, K., A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals?, Lab. Anim., 1990, vol. 24, no. 1, pp. 71–77. https://doi.org/10.1258/002367790780890347

    Article  PubMed  Google Scholar 

  77. Lajus, D., Graham, J.H., and Kozhara, A., Developmental instability and the stochastic component of total phenotypic variance, in Developmental Instability: Causes and Consequences, New York: Oxford University Press, 2003, pp. 343–363.

    Google Scholar 

  78. Forde, G.B., Is it good noise? The role of developmental instability in the shaping of a root system, J. Exp. Bot., 2009, vol. 60, no. 14, pp. 3989–4002. https://doi.org/10.1093/jxb/erp265

    Article  CAS  PubMed  Google Scholar 

  79. Shahrezaei, V. and Swain, P.S., The stochastic nature of biochemical networks, Cur. Opin. Biotech., 2008, vol. 19, no. 4, pp. 369–374. https://doi.org/10.1016/j.copbio.2008.06.011

    Article  CAS  Google Scholar 

  80. Ribeiro, A.S., Smolander, O., Rajala, T., Häkkinen, A., and Yli-Harja, O., Delayed stochastic model of transcription at the single nucleotide level, J. Comput. Biol., 2009, vol. 16, no. 4, pp. 539–553. https://doi.org/10.1089/cmb.2008.0153

    Article  CAS  PubMed  Google Scholar 

  81. Sigworth, F.J., Open channel noise. I. Noise in acetylcholine receptor currents suggests conformational fluctuations, Biophys. J., 1985, vol. 47, no. 5, pp. 709–720. https://doi.org/10.1016/S0006-3495(85)83968-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sangster, T.A., Salathia, N., Lee, H.N., Watanabe, E., Schellenberg, K., Morneau, K., Wang, H., Undurraga, S., Queitsch, C., and Lindquist, S., HSP90-buffered genetic variation is common in Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, no. 8, pp. 2969–2974. https://doi.org/10.1073/pnas.0712210105

    Article  PubMed  PubMed Central  Google Scholar 

  83. Borkovich, K.A., Ferrelly, F.W., Finkelstein, D.B., Tauliey, J., and Lindquist, S., Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures, Mol. Cell. Biol., 1989, vol. 9, no. 9, pp. 3919–3930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bandura, J.L., Jiang, H., Nickerson, D.W., and Edgar, B.A., The molecular chaperone Hsp90 is required for cell cycle exit in Drosophila melanogaster, PLoS Genet., 2013, vol. 9, no. 9, e1003835. https://doi.org/10.1371/journal.pgen.1003835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Prasinos, C., Krampis, K., Samakovli, D., and Hatzopoulos, P., Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development, J. Exp. Bot., 2005, vol. 56, no. 412, pp. 633–644. https://doi.org/10.1093/jxb/eri035

    Article  CAS  PubMed  Google Scholar 

  86. Oh, S.E., Yeung, C., Babaei-Rad, R., and Zhao, R., Cosuppression of the chloroplast localized molecular chaperone HSP90.5 impairs plant development and chloroplast biogenesis in Arabidopsis, BMC Res. Not., 2014, vol. 7, no. 1, 643. https://doi.org/10.1186/1756-0500-7-643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Yeyati, P.L., Bancewicz, R.M., Maule, J., and van Heyningen, V., Hsp90 selectively modulates phenotype in vertebrate development, PLoS Genet., 2007, vol. 3, no. 3, e43. https://doi.org/10.1371/journal.pgen.0030043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ali, A., Bharadwaj, S., O’Carroll, R., and Ovsenek, N., Hsp90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes, Mol. Cell. Biol., 1998, vol. 18, pp. 4949–4960. https://doi.org/10.1128/MCB.18.9.4949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Uversky, V.N., What does it mean to be natively unfolded?, Eur. J. Biochem., 2002, vol. 269, no. 1, pp. 2–12. https://doi.org/10.1046/j.0014-2956.2001.02649.x

    Article  CAS  PubMed  Google Scholar 

  90. Bradshow, A.D., Evolutionary significance of phenotypic plasticity in plants, Adv. Genet. 1965, vol. 13, no. 2, pp. 115–155. https://doi.org/10.1016/S0065-2660(08)60048-6

    Article  Google Scholar 

  91. Kordyum, E.L., Sytnik, K.M., Baranenko, V.V., Belyav-skaya, N.A., Klimchuk, D.A., and Nedukha, E.M., Cell Mechan. Plant Adapt. Adv. Environ. Factors Nat. Condit., Kiev: Naukova Dumka. 2003.

    Google Scholar 

  92. Slack, J.M.W., Conrad Hal Waddington: the last Renaissance biologist?, Nat. Rev. Genet., 2002, vol. 3, no. 11, pp. 889–895. https://doi.org/10.1038/nrg933

    Article  CAS  PubMed  Google Scholar 

  93. Lin, Y. and Cheng, C.L., A chlorate-resistant mutant defective in the regulation of nitrate reductase gene expression in Arabidopsis defines a new HY locus, Plant Cell, 1997, vol. 9, no. 1, pp. 21–35. https://doi.org/10.1105/tpc.9.1.21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Cao, D., Lin, Y., and Cheng, C.L., Genetic interactions between the chlorate-resistant mutant cr88 and the photomorphogenic mutants cop1 and hy5, Plant Cell, 2000, vol. 12, no. 2, pp. 199–210. https://doi.org/10.1105/tpc.12.2.199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Kitano, H., Biological robustness, Nat. Rev. Genet., 2004, vol. 5, no. 11, pp. 826–836. https://doi.org/10.1038/nrg1471

    Article  CAS  PubMed  Google Scholar 

  96. Kimura, M., Neutr. Theor. Mol. Evolut., New York: Cambridge Univ. Press, 1983.

    Book  Google Scholar 

  97. Mitchell-Olds, T. and Schmitt, J., Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis, Nature, 2006, vol. 441, no. 7096, pp. 947–952. https://doi.org/10.1038/nature04878

    Article  CAS  PubMed  Google Scholar 

  98. Sangster, T.A., Salathia, N., Undurraga, S., Milo, R., Schellenberg, K., Lindquist, S., and Queitsch, C., HSP90 affects the expression of genetic variation and development stability in quantitative traits, Proc. Natl. Acad. Sci. U. S. A. 2008, vol. 105, no. 8, pp. 2963–2968. https://doi.org/10.1073/pnas.0712200105

    Article  PubMed  PubMed Central  Google Scholar 

  99. Abbott, R.J. and Gomes, M.F., Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh., Heredity, 1989, vol. 62, no. 3, pp. 411–418. https://doi.org/10.1038/hdy.1989.56

    Article  Google Scholar 

  100. Koornneef, M., Dellaert, L.W.M., and Van Der Veen, J.H., EMS-induced and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh, Mutat. Res., 1982, vol. 93, no. 1, pp. 109–123. https://doi.org/10.1016/0027-5107(82)90129-4

    Article  CAS  PubMed  Google Scholar 

  101. Grodzinsky, D.M., Plant Radiobiology, Kiev: Naukova Dumka, 1989.

    Google Scholar 

  102. Grodzinsky, D.M., Dmitriev, O.P., Gusha, M.I., Kolomiets, O.D., Kravetz, O.A., and Rashydov, N.M., UV-B Radiation and Plants: Mechanisms of Damage and Protection, Kyiv: Fitosotsiotsentr, 2007.

    Google Scholar 

  103. Gorobchenko, O.A., Nikolov, O.T., and Gatash, S.V., Influence of γ-irradiation on thermal-evoked conformational transitions and hydration of fibrinogen, Biopol. Cell, 2006, vol. 22, no. 2, pp. 162–165. https://doi.org/10.7124/bc.00072C

    Article  CAS  Google Scholar 

  104. Kozeko L., Talalaiev O., Neimash V., Povarchuk V. A protective role of HSP90 chaperone in gamma-irradiated Arabidopsis thaliana seeds, Life Sci. Space Res. 2015, vol. 6, pp. 51–8. doi .https://doi.org/10.1016/j.lssr.2015.07.002

    Article  Google Scholar 

  105. Kozeko, L.Ye., Chaperones HSP90 as a stabilizer of plant growth and morphogenesis: a microevolutionary aspect, Fact. Exp. Evol. Organ., 2016, vol. 18, pp. 42–45.

    Google Scholar 

  106. Sollars, V., Lu, X., Xiao, L., Wang, X., Garfinkel, M.D., and Ruden, D.M., Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution, Nat. Genet., 2003, vol. 33, no. 1, pp. 70–74. https://doi.org/10.1038/ng1067

    Article  CAS  PubMed  Google Scholar 

  107. Specchia, V., Piacentini, L., Tritto, P., Fanti, L., D’Alessandro, R., Palumbo, G., Pimpinelli, S., and Bozzetti, M.P., Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons, Nature, 2010, vol. 463, no. 7281, pp. 662–665. https://doi.org/10.1038/nature08739

    Article  CAS  PubMed  Google Scholar 

  108. Ananthan, J., Goldberg, A.L., and Voellmy, R., Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes, Science, 1986, vol. 232, no. 4749, pp. 522–5224. https://doi.org/10.1126/science.3083508

    Article  CAS  PubMed  Google Scholar 

  109. Mathew, A. and Morimoto, R.I., Role of the heatshock response in the life and death of proteins, in Stress of Life from Molecules to Man, Ann. N.Y. Acad. Sci., 1998, vol. 851, pp. 99–111. https://doi.org/10.1111/j.1749-6632.1998.tb08982.x

    Article  CAS  PubMed  Google Scholar 

  110. Höhfeld, J., Cyr, D.M., and Patterson, C., From the cradle to the grave: molecular chaperones that may choose between folding and degradation, EMBO Rep., 2001, vol. 2, no. 10, pp. 885–890. https://doi.org/10.1093/embo-reports/kve206

    Article  PubMed  PubMed Central  Google Scholar 

  111. Wiech, H., Buchner, J., Zimmermann, R., and Jakob, U., Hsp90 chaperones protein folding in vitro, Nature, 1992, vol. 358, no. 6382, pp. 169–170. https://doi.org/10.1038/358169a0

    Article  CAS  PubMed  Google Scholar 

  112. Fernandes, M., O’brien, T., and Lis, J.T., Structure and regulation of heat shock gene promoters, in The Biology of Heat Shock Proteins and Molecular Chaperones, New York: Cold Spring Harbor Laboratory Press, 1994, pp. 375–393. https://doi.org/10.1101/087969427.26.375

    Google Scholar 

  113. Akerfelt, M., Morimoto, R.I., and Sistonen, L., Heat shock factors: integrators of cell stress, development and lifespan, Nat. Rev. Mol. Cell Biol., 2010, vol. 11, no. 8, pp. 545–555. https://doi.org/10.1038/nrm2938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. McLellan, C.A., Turbyville, T.J., Wijeratne, E.M., Kerschen, A., Vierling, E., Queitsch, C., Whitesell, L., and Gunatilaka, A.A., A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor, Plant Physiol., 2007, vol. 145, no. 1, pp. 174–182. https://doi.org/10.1104/pp.107.101808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Kozeko, L.Ye., Changes in heat-shock protein synthesis and thermotolerance of Arabidopsis thaliana seedlings resulting from Hsp90 inhibition by geldanamycin, Cell Tiss. Biol., 2014, vol. 8, no. 5, pp. 416–422. https://doi.org/10.1134/S1990519X14050046

    Article  Google Scholar 

  116. von Koskull-Döring, P., Scharf, K.D., and Nover, L., The diversity of plant heat stress transcription factors, Trends Plant Sci., 2007, vol. 12, no. 10, pp. 452–457. https://doi.org/10.1016/j.tplants.2007.08.014

    Article  CAS  PubMed  Google Scholar 

  117. Schramm, F., Larkindale, J., Kiehlmann, E., Ganguli, A., Englich, G., Vierling, E., and von Koskull-Doring, P., A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis, Plant J., 2008, vol. 53, no. 2, pp. 264–274. https://doi.org/10.1111/j.1365-313X.2007.03334.x

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, 01601, Kyiv, Ukraine

    L. Y. Kozeko

Authors
  1. L. Y. Kozeko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Y. Kozeko.

Additional information

Translated by K. Lazarev

Supplementary materials are available for this article at DOI: 10.3103/S0095452719020063 and are accessible for authorized users.

Supplementary material

COMPLIANCE WITH ETHICAL STANDARDS

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kozeko, L.Y. The Role of HSP90 Chaperones in Stability and Plasticity of Ontogenesis of Plants under Normal and Stressful Conditions (Arabidopsis thaliana). Cytol. Genet. 53, 143–161 (2019). https://doi.org/10.3103/S0095452719020063

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452719020063

Keywords:

Search

Navigation