Abstract
Higher plants have acquired complex molecular mechanisms to withstand heat stress through years of natural evolutionary processes. Although physiological responses to elevated temperatures have been well studied, thermotolerance mechanisms at the molecular level are poorly understood in rice plants. In order to identify the genes involved in the thermotolerance of rice, we used a publicly available microarray dataset and identified a number of heat stress-responsive genes. Herein, we report details of the rice gene OsHSP1, which is upregulated by heat stress. In addition, OsHSP1 is highly expressed when exposed to salt and osmotic treatments but not cold treatment. Sequence analysis indicated that OsHSP1 belongs to the heat shock protein 90 family of genes. The biological function of OsHSP1 was investigated by heterologous overexpression in Arabidopsis. Transgenic Arabidopsis overexpressing the OsHSP1 gene exhibited enhanced thermotolerance but was hypersensitive under salt and osmotic stresses. Subcellular localization analysis indicated that the OsHSP1 protein is predominantly targeted to the cytosol and nucleus under heat stress. The coexpression network showed 39 interactions for the functionally interacting genes of OsHSP1. Taken together, these findings suggest that OsHSP1 is a heat-inducible gene that may play an important role in the thermotolerance of rice.
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Altieri DC, Stein GS, Lian JB, Languino LR (2012) TRAP-1, the mitochondrial Hsp90. BBA-Mol Cell Res 1823:767–773
Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222
Cao D, Froehlich JE, Zhang H, Cheng C-L (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33:107–118
Dat JF, Foyer CH, Scott IM (1998a) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461
Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998b) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357
Ham D-J, Moon J-C, Hwang S-G, Jang CS (2013) Molecular characterization of two small heat shock protein genes in rice: their expression patterns, localizations, networks, and heterogeneous overexpressions. Mol Biol Rep. doi:10.1007/s11033-013-2786-x
Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590
Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 22:5679–5689
Imai T, Kato Y, Kajiwara C, Mizukami S, Ishige I, Ichiyanagi T, Hikida M, Wang J-Y, Udono H (2011) Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proc Natl Acad Sci USA 108:16363–16368
Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61:143–156
Jung CG, Lim SD, Hwang S-G, Jang CS (2012) Molecular characterization and concerted evolution of two genes encoding RING-C2 type proteins in rice. Gene 505:9–18
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
Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperon 6:238–246
Langfelder P, Zhang B, Horvath S (2008) Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24:719–720
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695
Larkindale J, Michael M, Elizabeth V (2005) Plant responses to high temperature. In: Jenks MA, Hasegawa PM (eds) Plant Abiotic Stress. Blackwell Publishing, Oxford, pp 100–144
Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) 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 279:2101–2108
Lohmann C, Eggers-Schumacher G, Wunderlich M, Schöffl F (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol Genet Genomics 271:11–21
Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu A-J, 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
Marzec M, Eletto D, Argon Y (2012) GRP94: an HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. BBA-Mol Cell Res 1823:774–787
Mauch-mani B, Métraux J-p (1998) Salicylic Acid and Systemic Acquired Resistance to Pathogen Attack. Ann Bot 82:535–540
Pearl LH, Prodromou C (2000) Structure and in vivo function of Hsp90. Curr Opin Struct Biol 10:46–51
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proce Natl Acad Sci USA 101:9971–9975
Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res 13:2498–2504
Snyman M, Cronjé MJ (2008) Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J Exp Bot 59:2125–2132
Sung DY, Vierling E, Guy CL (2001) Comprehensive Expression Profile Analysis of the Arabidopsis Hsp70 Gene Family. Plant Physiol 126:789–800
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
Verslues PE, Bray EA (2004) LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis. Plant Physiol 136:2831–2842
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Wiech H, Buchner J, Zimmermann R, Jakob U (1992) Hsp90 chaperones protein folding in vitro. Nature 358:169–170
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 282:37794–37804
Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4:Article17
Zhang X, Henriques R, Lin S-S, Niu Q-w, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protoc 1:641–646
Acknowledgments
This research was supported by iPET (Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries), Ministry for Food, Agriculture, Forestry and Fisheries and a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center No. PJ009084), Rural Development Administration, Republic of Korea.
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Moon, JC., Ham, D.J., Hwang, SG. et al. Molecular characterization of a heat inducible rice gene, OsHSP1, and implications for rice thermotolerance. Genes Genom 36, 151–161 (2014). https://doi.org/10.1007/s13258-013-0152-y
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DOI: https://doi.org/10.1007/s13258-013-0152-y