Skip to main content
Log in

Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Three AtHsp90 isoforms, cytosolic AtHsp90.2, chloroplast-located AtHsp90.5, and endoplasmic reticulum (ER)-located AtHsp90.7, were characterized by constitutive overexpressing their genes in Arabidopsis thaliana. Both types of the transgenic plants overexpressing cytosolic and organellar AtHsp90s showed reduced tolerance to salt and drought stresses with lower germination rates and fresh weights, but improved tolerance to high concentration of Ca2+ comparing with the wild type plants. Transcriptional analysis of ABA-responsive genes, RD29A, RD22 and KIN2 under salt and drought stresses, indicated that the induction expression of these genes was delayed by constitutive overexpression of cytosolic AtHsp90.2, but was hardly affected by that of organellar AtHsp90.5 and AtHsp90.7. These results implied that Arabidopsis different cellular compartments-located Hsp90s in Arabidopsis might be involved in abiotic stresses by different functional mechanisms, probably through ABA-dependent or Ca2+ pathways, and proper homeostasis of Hsp90 was critical for cellular stress response and/or tolerance in plants.

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

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CaMV:

Cauliflower mosaic virus

Hsc:

Cognate form of Hsp

Hsp:

Heat shock protein

MAPK:

Mitogen-activated protein kinase

ROS:

Reactive oxygen species

UPR:

Unfolded protein response

References

  • Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol 144:312–323

    Article  PubMed  CAS  Google Scholar 

  • Cao D, Froehlich JE, Zhang H, Cheng CL (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted Hsp90. Plant J 33:107–118

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Czar M, Galigniana M, Silverstein A, Pratt W (1997) Geldanamycin, a heat shock protein 90-binding steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus. Biochemistry 36:7776–7785

    Article  PubMed  CAS  Google Scholar 

  • García-Cardeña G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC (1998) Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392:821–824

    Article  PubMed  Google Scholar 

  • Gilmour SJ, Lin C, Thomashow MF (1996) Purification and properties of Arabidopsis thaliana COR (cold-regulated) gene polypeptides CORl5am and COR6.6 expressed in Escherichia coli. Plant Physiol 111:293–299

    Article  PubMed  CAS  Google Scholar 

  • Hawle P, Horst D, Bebelman JP, Yang XX, Siderius M, van der Vies SM (2007) Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot Cell 6:521–532

    Article  PubMed  CAS  Google Scholar 

  • Hogan PG, Li H (2005) Calcineurin. Curr Biol 15:R442–R443

    Article  PubMed  CAS  Google Scholar 

  • Holt SE, Aisner DL, Baur J, Tesmer VM, Dy M, Ouellette M, Trager JB, Morin GB, Toft DO, Shay JW, Wright WE, White MA (1999) Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev 13:817–826

    Article  PubMed  CAS  Google Scholar 

  • Imai J, Yahara I (2000) Role of Hsp90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20:9262–9270

    Article  PubMed  CAS  Google Scholar 

  • Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H, Okada K (2002) SHEPHERD is the Arabidopsis Grp94 responsible for the formation of functional clavata proteins. EMBO J 21:898–908

    Article  PubMed  CAS  Google Scholar 

  • 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. Mol Plant Pathol 4:383–391

    Article  CAS  Google Scholar 

  • Klein EM, Mascheroni L, Pompa A, Ragni L, Weimar T, Lilley KS, Paul D, Alessandro V (2006) Plant endoplasmin supports the protein secretory pathway and has a role in proliferating tissues. Plant J 48:657–673

    Article  PubMed  CAS  Google Scholar 

  • Koning AJ, Rose R, Comai L (1992) Developmental expression of tomato heat-shock cognate protein 80. Plant Physiol 100:801–811

    Article  PubMed  CAS  Google Scholar 

  • Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  PubMed  CAS  Google Scholar 

  • Krishna P, Reddy RK, Sacco M, Frappier JR, Felsheim RF (1997) Analysis of the native forms of the 90 kda heat shock protein (Hsp90) in plant cytosolic extracts. Plant Mol Biol 33:457–466

    Article  PubMed  CAS  Google Scholar 

  • Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1996) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723

    Article  Google Scholar 

  • Kurkela S, Borg-Franck M (1992) Structure and expression of KIN2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19:689–692

    Article  PubMed  CAS  Google Scholar 

  • Lee MW, Lee HJ, Bach JH, Park SC, Park JS, Lee KG, Yeo JH, Lee WB, Lee SH, Kim SS (2005) Down-regulated reactive oxygen species by HSP90 in 3HK-induced SKN-SH cell death. J Therm Biol 30:43–49

    Article  CAS  Google Scholar 

  • Liu D, Zhang X, Cheng Y, Takano T, Liu S (2006) rHsp90 gene expression in response to several environmental stresses in rice (Oryza sativa L.). Plant Physiol Biochem 44:380–386

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

    Article  PubMed  CAS  Google Scholar 

  • Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen JP, Bendahmane A, Day L, Baulcombe DC (2003) High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22:5690–5699

    Article  PubMed  CAS  Google Scholar 

  • Marrs KA, Casey ES, Capitant SA, Bouchard RA, Dietrich PS, Mettler IJ, Sinibaldi RM (1993) Characterization of two maize Hsp90 heat shock protein genes: Expression during heat shock, embryogenesis and pollen development. Dev Genet 14:27–41

    Article  PubMed  CAS  Google Scholar 

  • Marcu MG, Doyle M, Bertolotti A, Ron D, Hendershot L, Neckers L (2002) Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1α. Mol Cell Biol 22:8506–8513

    Article  PubMed  CAS  Google Scholar 

  • Milioni D, Hatzopoulos P (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955–961

    Article  PubMed  CAS  Google Scholar 

  • Millson SH, Truman AW, King V, Prodromou C, Pearl LH, Piper PW (2005) A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot Cell 4:849–860

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94:12949–12956

    Article  PubMed  CAS  Google Scholar 

  • Pandey GK, Cheong YH, Kim K-N, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924

    Article  PubMed  CAS  Google Scholar 

  • Pearl LH, Prodromou C (2000) Structure and in vivo function of Hsp90. Curr Opin Struct Biol 10:46–51

    Article  PubMed  CAS  Google Scholar 

  • Prassinos C, Haralampidis K, Milioni D, Samakovli D, Krambis K, Hatzopoulos P (2008) Complexity of Hsp90 in organelle targeting. Plant Mol Biol 67:323–334

    Article  PubMed  CAS  Google Scholar 

  • Pratt WB, Krishna P, Olsen LJ (2001) Hsp90-binding immunophilins in plants: the protein movers. Trends Plant Sci 6:54–58

    Article  PubMed  CAS  Google Scholar 

  • Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–625

    Article  PubMed  CAS  Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342

    Article  PubMed  CAS  Google Scholar 

  • Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS ONE 7:1–14

    Google Scholar 

  • Sangster TA, Queitsch C (2005) The Hsp90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr Opin Plant Biol 8:86–92

    Article  PubMed  CAS  Google Scholar 

  • Sangster TA, Lindquist S, Queitsch C (2004) Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays 26:348–362

    Article  PubMed  CAS  Google Scholar 

  • Schroder G, Beck M, Eichel J, Vetter HP, Schroder J (1993) Hsp90 homologue from madagascar periwinkle (Catharanthus roseus): cDNA sequence, regulation of protein expression and location in the endoplasmic reticulum. Plant Mol Biol 23:583–594

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Takahashi T, Naito S, Komeda Y (1992) Isolation and analysis of the expression of two genes for the 81-kilodalton heat-shock proteins from Arabidopsis. Plant Physiol 99:383–390

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993a) Characterization of the expression of a desiccation-responsive RD29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993b) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of RD22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25

    PubMed  CAS  Google Scholar 

  • Yang XX, Maurer KCT, Molanus M, Mager WH, Siderius M, van der Vies SM (2006) The molecular chaperone Hsp90 is required for high osmotic stress response in Saccharomyces cerevisiae. FEMS Yeast Res 6:195–204

    Article  PubMed  CAS  Google Scholar 

  • Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154:267–273

    Article  PubMed  CAS  Google Scholar 

  • Zhao RM, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan G, Cagney D, Mai JG (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the Hsp90 chaperone. Cell 120:715–727

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Walid Houry (University of Toronto, Canada) for providing us with polyclonal antibody against yeast Hsp82 protein. This work is supported by the National Natural Science Foundation of China (Grant No.30470352) and the National High Technology and Research Development Program of China (“863” project, Grant No. 2007AA091705).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Rongmin Zhao or Yinxin Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, H., Zhao, R., Fan, P. et al. Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229, 955–964 (2009). https://doi.org/10.1007/s00425-008-0886-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0886-y

Keywords

Navigation