Abstract
Three AtHSP90 isoforms, cytosol-localized AtHSP90.2, chloroplast-localized AtHSP90.5, and endoplasmic reticulum (ER)-localized AtHSP90.7 genes, were constitutively overexpressed in Arabidopsis thaliana to study their functional mechanisms under oxidative stress. Overexpression of AtHSP90 genes reduced germination of transgenic seeds under oxidative stress. When exposed to 10 mM H2O2, AtHSP90 transgenic seedlings displayed lower activities of superoxide dismutase, catalase, and peroxidase; higher content of malondialdehyde; and higher levels of protein damage than detected in the wild type. This indicated that overexpression of AtHSP90.2, AtHSP90.5, and AtHSP90.7 in Arabidopsis impaired plant tolerance to oxidative stress. Moreover, overexpression of chloroplast- and ER-localized AtHSP90 resulted in lower resistance to oxidative stress than that of cytosolic AtHSP90. This suggested that HSP90.2, HSP90.5, and HSP90.7 localized in different cellular compartments were involved in different functional mechanisms during oxidative stress.
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Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396. doi:10.1104/pp.106.082040
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Campo S, Carrascal M, Coca M, Abian J, Segundo BS (2004) The defense response of germinating maize embryos against fungal infection: a proteomics approach. Proteomics 4:383–396. doi:10.1002/pmic.200300657
Cao DS, Forehlich JE, Zhang H, Cheng CL (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33:107–118. doi:10.1046/j.1365-313X.2003.016011.x
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x
Desikan R, A-H-Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172. doi:10.1104/pp.127.1.159
Ellis RJ (1990) The molecular chaperone concept. Semin Cell Biol 1:1–9
Ghezzi P, Bonetto V (2003) Redox proteomics: identification of oxidatively modified proteins. Proteomics 3:1145–1153. doi:10.1002/pmic.200300435
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, London
Hernandez JA, Ferrer MA, Jimenez A, Barcelo AR, Sevilla F (2001) Antioxidant systems and O −2 /H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:827–831. doi:10.1104/pp. 010188
Imai J, Yahara I (2000) Role of HSP90 in salt stress tolerance via stabilization and regulation of calcineurin. Mol Cell Biol 20:9262–9270. doi:10.1128/MCB.20.24.9262-9270.2000
Ippolito A, Ghaouth AE, Wilson CL, Wisniewski M (2000) Control of postharvest decay of apple fruit by Aureobasidium pullulans and induction of defense responses. Postharvest Biol Technol 19:265–272. doi:10.1016/S0925-5214(00)00104-6
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. doi:10.1093/emboj/21.5.898
Jackson SE, Queitsch C, Toft D (2004) HSP90: from structure to phenotype. Nat Struct Mol Biol 11:1152–1156. doi:10.1038/nsmb1204-1152
Kimura Y, Matsumoto S, Yahara I (1994) Temperature-sensitive mutants of hsp82 of the budding yeast Saccharomyces cerevisiae. Mol Gen Genet 242:517–527. doi:10.1007/BF00285275
Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246. doi:10.1379/1466-1268(2001)006<0238:THFOPI>2.0.CO;2
Krishna P, Sacco M, Cherutti JF, Hill S (1995) Cold-induced accumulation of HSP90 transcripts in Brassica napus. Plant Physiol 107(91):95–923
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 44:380–386. doi:10.1016/j.plaphy.2006.06.011
Ma Y, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28:51–65. doi:10.1016/j.jchemneu.2003.08.007
Milioni D, Hatzopoulos P (1997) Genomic organization of HSP90 gene family in Arabidopsis. Plant Mol Biol 35:955–961. doi:10.1023/A:1005874521528
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Murata S, Minami Y, Minami M, Chiba T, Tanaka K (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2:1133–1138. doi:10.1093/embo-reports/kve246
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. doi:10.1146/annurev.arplant.49.1.249
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 29:293–301. doi:10.1007/BF00043653
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. doi:10.1007/s11103-008-9322-8
Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the HSP90/HSP70-based chaperone machinery. Exp Biol Med 228:111–133
Ree I, Lee S, Kim H, Tsai FTF (2006) The E3 ubiquitin ligase CHIP binds the androgen receptor in a phosphorylation-dependent manner. Biochim Biophys Acta 1764:1073–1079
Sangster TA, Lindquist S, Queitsch C (2004) Under cover: causes, effects and implications of HSP90-mediated genetic capacitance. BioEssays 26:348–362. doi:10.1002/bies.20020
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
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 229:955–964
Wang YS, Tian SP, Xu Y (2005) Effects of high oxygen concentration on pro- and anti-oxidant enzymes in peach fruit during postharvest periods. Food Chem 91:99–104. doi:10.1016/j.foodchem.2004.05.053
Xu CY, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. Clin Invest Med 115:2656–2664. doi:10.1172/JCI26373
Xu XB, Tian SP (2008) Salicylic acid alleviated pathogen-induced oxidative stress in harvested sweet cherry fruit. Postharvest Biol Technol 49:379–85. doi:10.1016/j.postharvbio.2008.02.003
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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).
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Song, H., Fan, P. & Li, Y. Overexpression of Organellar and Cytosolic AtHSP90 in Arabidopsis thaliana Impairs Plant Tolerance to Oxidative Stress. Plant Mol Biol Rep 27, 342–349 (2009). https://doi.org/10.1007/s11105-009-0091-6
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DOI: https://doi.org/10.1007/s11105-009-0091-6