Skip to main content
Log in

Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The ROF2 (FKBP65) is a heat stress protein which belongs to the FK506 Binding Protein (FKBP) family. It is homologous to ROF1 (FKBP62) which was recently shown to be involved in long term acquired thermotolerance by its interaction with HSP90.1 and modulation of the heat shock transcription factor HsfA2. In this study, we have demonstrated that ROF2 participates in long term acquired thermolerance, its mode of action being different from ROF1. In the absence of ROF2, the small heat shock proteins were highly expressed and the plants were resistant to heat stress, opposite to the effect observed in the absence of ROF1. It was further demonstrated that ROF2 transcription is modulated by HsfA2 which is also essential for keeping high levels of ROF2 during recovery from heat stress. ROF2 localization to the nucleus was observed several hours after heat stress exposure and its translocation to the nucleus was independent from the presence of HSP90.1 or HsfA2. ROF2 has been shown to interact with ROF1, to form heterodimers and it is suggested that via this interaction it can join the complex ROF1-HSP90.1- HsfA2. Transient expression of ROF2 together with ROF1 repressed transcription of small HSPs. A model describing the mode of action of ROF2 as a heat stress modulator which functions in negative feedback regulation of HsfA2 is proposed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

FKBP:

FK506-binding protein

PPIase:

Peptidyl prolyl cistrans isomerase

TPR:

Tripartite tetratricopeptide repeats

HSP:

Heat shock protein

HSF:

Heat shock factor

HSE:

Heat shock element

References

  • Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, von Koskull-Doring P, Ohad N, Breiman A (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63:237–255

    Article  CAS  PubMed  Google Scholar 

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826

    Article  CAS  PubMed  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Doring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    Article  CAS  PubMed  Google Scholar 

  • Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A (1996) A novel plant peptidyl-prolyl-cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol Biol 32:493–504

    Article  CAS  PubMed  Google Scholar 

  • Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281:30603–30612

    Article  CAS  PubMed  Google Scholar 

  • Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, Yalovsky S, Ohad N (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40:419–427

    Article  CAS  PubMed  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262

    Article  CAS  PubMed  Google Scholar 

  • Dafny-Yelin M, Tzfira T, Vainstein A, Adam Z (2008) Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Mol Biol 67:363–373

    Article  CAS  PubMed  Google Scholar 

  • Davies TH, Ning YM, Sanchez ER (2002) A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J Biol Chem 277:4597–4600

    Article  CAS  PubMed  Google Scholar 

  • Faure JD, Gingerich D, Howell SH (1998) An Arabidopsis immunophilin, AtFKBP12, binds to AtFIP37 (FKBP interacting protein) in an interaction that is disrupted by FK506. Plant J 15:783–789

    Article  CAS  PubMed  Google Scholar 

  • Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337:476–478

    Article  CAS  PubMed  Google Scholar 

  • Galat A (2003) Peptidyl prolyl cis/trans isomerases (immunophilins): biological diversity–targets–functions. Curr Top Med Chem 3:1315–1347

    Article  CAS  PubMed  Google Scholar 

  • Gallo LI, Ghini AA, Pilipuk GP, Galigniana MD (2007) Differential recruitment of tetratricorpeptide repeat domain immunophilins to the mineralocorticoid receptor influences both heat-shock protein 90-dependent retro transport and hormone-dependent transcriptional activity. Biochemistry 46:14044–14057

    Article  CAS  PubMed  Google Scholar 

  • Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends Plant Sci 12:465–473

    Article  CAS  PubMed  Google Scholar 

  • Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu UH, Schulz B, Martinoia E (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15:3393–3405

    Article  CAS  PubMed  Google Scholar 

  • Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27:25–35

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Katyar-Agarwal S, Agarwal M, Grover A (2003) Heat tolerant basmati rice engineered by overexpression of Hsp101. Plant Mol Biol 51:677–686

    Article  Google Scholar 

  • Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. Embo J 22:4804–4814

    Article  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • Kurek I, Aviezer K, Erel N, Herman E, Breiman A (1999) The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol 119:693–704

    Article  CAS  PubMed  Google Scholar 

  • Kurek I, Pirkl F, Fischer E, Buchner J, Breiman A (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis-trans isomerase activity. Planta 215:119–126

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    Article  CAS  PubMed  Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI (2002) Dynamic remodeling of transcription complexes by molecular chaperones. Cell 110:281–284

    Article  CAS  PubMed  Google Scholar 

  • Morimoto RI, Santoro MG (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16:833–838

    Article  CAS  PubMed  Google Scholar 

  • Nieto-Sotelo J, Martinez LM, Ponce G, Cassab GI, Alagon A, Meeley RB, Ribaut JM, Yang R (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell 14:1621–1633

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nover L, Scharf KD (1997) Heat stress proteins and transcription factors. Cell Mol Life Sci 53:80–103

    Article  CAS  PubMed  Google Scholar 

  • Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383

    Article  CAS  PubMed  Google Scholar 

  • Pirkl F, Fischer E, Modrow S, Buchner J (2001) Localization of the chaperone domain of FKBP52. J Biol Chem 276:37034–37041

    Article  CAS  PubMed  Google Scholar 

  • Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306–360

    Article  CAS  PubMed  Google Scholar 

  • Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492

    Article  CAS  PubMed  Google Scholar 

  • Reddy RK, Kurek I, Silverstein AM, Chinkers M, Breiman A, Krishna P (1998) High-molecular-weight FK506-binding proteins are components of heat-shock protein 90 heterocomplexes in wheat germ lysate. Plant Physiol 118:1395–1401

    Article  CAS  PubMed  Google Scholar 

  • Riggs DL, Roberts PJ, Chirillo SC, Cheung-Flynn J, Prapapanich V, Ratajczak T, Gaber R, Picard D, Smith DF (2003) The Hsp90-binding peptidy lprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J 22:1158–1167

    Article  CAS  PubMed  Google Scholar 

  • Schoffl F, Prandl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiol 117:1135–1141

    Article  CAS  PubMed  Google Scholar 

  • Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, von Koskull-Doring 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

    Article  CAS  PubMed  Google Scholar 

  • Siddique M, Gernhard S, von Koskull-Doring P, Vierling E, Scharf KD (2008) The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13:183–197

    Article  CAS  PubMed  Google Scholar 

  • Smith DF, Toft DO (2008) Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Mol Endocrinol 22:2229–2240

    Article  CAS  PubMed  Google Scholar 

  • Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure JD (2006) The C terminus of the immunophilin PASTICCINO1 is required for plant development and for interaction with a NAC-like transcription factor. J Biol Chem 281:25475–25484

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100:11777–11782

    Article  CAS  PubMed  Google Scholar 

  • Tonsor SJ, Scott C, Boumaza I, Liss TR, Brodsky JL, Vierling E (2008) Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Mol Ecol 17:1614–1626

    Article  CAS  PubMed  Google Scholar 

  • Vespa L, Vachon G, Berger F, Perazza D, Faure JD, Herzog M (2004) The immunophilin-interacting protein AtFIP37 from Arabidopsis is essential for plant development and is involved in trichome endoreduplication. Plant Physiol 134:1283–1292

    Article  CAS  PubMed  Google Scholar 

  • Vierling E, Kimpel JA (1992) Plant responses to environmental stress. Curr Opin Biotechnol 3:164–170

    Article  CAS  PubMed  Google Scholar 

  • von Koskull-Doring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12:452–457

    Article  Google Scholar 

  • Waters ER, Schaal BA (1996) Heat shock induces a loss of rRNA-encoding DNA repeats in Brassica nigra. Proc Natl Acad Sci USA 93:1449–1452

    Article  CAS  PubMed  Google Scholar 

  • Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227:957–967

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. von Koskull-Doring, Cell Biology Goethe University Frankfurt for antibodies of HsfA2 and for the HsfA2 T-DNA insertion lines Dr. Adam Institute of Plant Genetics, Hebrew University Rehovot, for antibodies of sHSP-CI. We thank Dr. Shirasu for the AtHSP90.1 T-DNA insertion lines. We thank Moran Oliva for helping with the Nuclei Isolation. We thank the Institute for Crop Improvement in Tel Aviv University for plant growing facilities. The work was supported by a grant from the Israeli National Academy of Science to A. Breiman.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adina Breiman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meiri, D., Tazat, K., Cohen-Peer, R. et al. Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol Biol 72, 191–203 (2010). https://doi.org/10.1007/s11103-009-9561-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-009-9561-3

Keywords

Navigation