Biotechnology Letters

, Volume 32, Issue 7, pp 979–987 | Cite as

Functional characterization of AtHsp90.3 in Saccharomyces cerevisiae and Arabidopsis thaliana under heat stress

  • Xiangbin Xu
  • Hongmiao Song
  • Zhenhua Zhou
  • Nongnong Shi
  • Qicai Ying
  • Huizhong Wang
Original Research Paper


The function of cytosolic AtHsp90.3 was characterized by complementing the Saccharomyces cerevisiae endogenous Hsp90 genes and overexpressing it in Arabidopsis thaliana. Though AtHsp90.3 supported the yeast growth under heat stress, in Arabidopsis, compared to the wild type, the transgenic plants overexpressing cytosolic AtHsp90.3 were more sensitive to heat stress with a lower germination rate and higher mortality but and more tolerant to high Ca2+. Transcriptional expression of heat stress transcription factors, AtHsfA1d, AtHsfA7a and AtHsfB1, and two Hsps, AtHsp101 and AtHsp17, was delayed by constitutive overexpression of cytosolic AtHsp90.3 under heat stress. These results indicate that overexpressing AtHsp90.3 impaired plant tolerance to heat stress and proper homeostasis of Hsp90 was critical for cellular stress response and/or tolerance in plants.


Arabidopsis thaliana Functional expression Heat shock protein 90 Heat stress 



This work is supported by the National Natural Science Foundation of China (30670199, 30870180 and 30770185), China Transgenic Plant Research and Commercialization Project (2009ZX08001-022B), the Zhejiang Scientific and Technological Program (2008C12081), the Natural Science Foundation of Zhejiang Province (No. Y3090426) and the Hangzhou Scientific and Technological Program (20080432T06, 20090233T15).


  1. Duina AA, Kalton HM, Gaber RF (1998) Requirement for Hsp90 and a CyP-40-type cyclophilin in negative regulation of the heat shock response. J Biol Chem 273:18974–18978CrossRefPubMedGoogle Scholar
  2. Gong M, Chen SN, Song YQ, Li ZG (1997) Effect of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust J Plant Physiol 24:373–379CrossRefGoogle Scholar
  3. 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 6:521–532CrossRefPubMedGoogle Scholar
  4. Imai J, Yahara I (2000) Role of Hsp90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20:9262–9270CrossRefPubMedGoogle Scholar
  5. Kimura Y, Matsumoto S, Yahara I (1994) Temperature-sensitive mutants of hsp82 of the budding yeast Saccharomyces cerevisiae. Mol Gen Genet 242:517–527CrossRefPubMedGoogle Scholar
  6. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246CrossRefPubMedGoogle Scholar
  7. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin b-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723CrossRefPubMedGoogle Scholar
  8. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945CrossRefPubMedGoogle Scholar
  9. Liu D, Zhang X, Cheng Y, Takano T, Liu S (2006) rHsp90 gene is in response to several environmental stresses in rice (Oryza sativa L.). Plant Physiol Biochem 44:380–386CrossRefPubMedGoogle Scholar
  10. Lynch J, Polito VS, Läuchli A (1989) Salinity stress increases cytoplasmic Ca activity in maize toot protoplasts. Plant Physiol 90:1271–1274CrossRefPubMedGoogle Scholar
  11. 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 22:8506–8513CrossRefPubMedGoogle Scholar
  12. Milioni D, Hatzopoulos P (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955–961CrossRefPubMedGoogle Scholar
  13. 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 4:849–860CrossRefPubMedGoogle Scholar
  14. Miroshnichenko S, Tripp J, Nieden U, Neumann D, Conrad U, Manteuffel R (2005) Immunomodulation of function of small heat shock proteins prevents their assembly into heat stress granules and results in cell death at sublethal temperatures. Plant J 41:269–281CrossRefPubMedGoogle Scholar
  15. Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16:1555–1567CrossRefPubMedGoogle Scholar
  16. Pareek A, Singla S, Grover A (1995) Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stresses in rice and in response to high temperature stress in diverse plant genera. Plant Mol Biol 29:293–301CrossRefPubMedGoogle Scholar
  17. Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med 228:111–133Google Scholar
  18. Price AH, Tayler A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310CrossRefPubMedGoogle Scholar
  19. Queitsch C, Hong SK, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492CrossRefPubMedGoogle Scholar
  20. Schramm F, Larkindale J, Kiehlmann E, Ganguli A, Englich G, Vierling E, von Koskull-Döring P (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53:264–274CrossRefPubMedGoogle Scholar
  21. Song HM, Zhao RM, Fan PX, Wang XC, Chen XY, Li YX (2009) Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229:955–964CrossRefPubMedGoogle Scholar
  22. 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 100:11777–11782CrossRefPubMedGoogle Scholar
  23. Xu XB, Tian SP (2008) Salicylic acid alleviated pathogen-induced oxidative stress in harvested sweet cherry fruit. Postharvest Biol Tech 49:379–385CrossRefGoogle Scholar
  24. Yamada K, Fukao Y, Hayashi M, Fukazawa M, Suzuki I, Nishimura M (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J Biol Chem 282:37794–37804CrossRefPubMedGoogle Scholar
  25. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R (1998) Repression of Heat Shock Transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:471–480CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Xiangbin Xu
    • 1
  • Hongmiao Song
    • 1
    • 2
  • Zhenhua Zhou
    • 1
  • Nongnong Shi
    • 1
  • Qicai Ying
    • 1
  • Huizhong Wang
    • 1
  1. 1.College of Life and Environmental SciencesHangzhou Normal UniversityHangzhouChina
  2. 2.The Institute of Crop and Nuclear Technology UtilizationZhejiang Academy of Agricultural SciencesHangzhouChina

Personalised recommendations