Plant Mol Biol Rep(2011)29:723-732 731 mitochondria that will result in the cell progressed death Magnard JL,Vergne P,Dumas C (1996)Complexity and genetic during flower development and then the sterility. variability of heat-shock protein expression in isolated maize microspores.Plant Physiol 111:1085-1096 Marino R,Pinto MR,Cotelli F,Lamia CL,De Santis R(1998)The hsp70 Acknowledgments This work was supported by 973 Program protein is involved in the acquisition of gamete self-sterility in the (2009CB119001-04)and Program for New Century Excellent Talents ascidian Ciona intestinalis.Development 125:899-907 in University (NCET-07-0439). Marrs KA,Casey ES,Capitant SA.Bouchard RA,Dietrich PS. Mettler IJ,Sinibaldi RM(1993)Characterization of two maize hsp90 heat shock protein genes and expression during heat References shock,embryogenesis and pollen development.Dev Genet 14:27-41 Mery DY,Tzvi T,Alexander V,Zach A (2008)Non-redundant Brown MA,Zhu L,Schmidt C,Tucker PW(2007)Hsp90-From signal functions of sHSP-CIs in acquired thermotolerance and their role transduction to cell transformation.Biochem Biophys Res in early seed development in Arabidopsis.Plant Mol Biol Commun363:241-246 67:363-373 Cao ZP.Jia ZW,Liu YJ,Wang M.Zhao JF,Zheng J.Wang GY(2009) Milioni D,Hatzopoulos P(1997)Genomic organization of hsp90 gene Constitutive expression of ZmsHSP in Arabidopsis enhances family in Arabidopsis.Plant Mol Biol 35:955-961 their cytokinin sensitivity.Mol Biol Rep 10:1089-1097 Muller L,Schaupp A,Walerych D,Wegele H,Buchner J(2004) Dafny-Yelin M,Guterman I,Menda N,Ovadis M,Shalit M,Pichersky Hsp90 regulates the activity of wild type p53 under physiological E,Zamir D,Lewinsohn E,Adam Z,Weiss D,Vainstein A(2005) and elevated temperatures.J Biol Chem 279:48846-48854 Flower proteome:changes in protein spectrum during the Pearl LH.Prodromou C(2006)Structure and mechanism of the Hsp90 advanced stages of rose petal development.Planta 222:37-46 molecular chaperone machinery.Annu Rev Biochem 75:271-294 Dafny-Yelin M,Tzfira T,Vainstein A.Adam Z(2008)Non-redundant Perez DE,Hoyer JS,Johnson Al,Moody ZR,Lopez J,Kaplinsky NJ functions of sHSP-CIs in acquired thermotolerance and their role in (2008)BOBBERI is a noncanonical Arabidopsis small heat early seed development in Arabidopsis.Plant Mol Biol 67:363-373 shock protein required for both development and thermotoler- Deng XH.Zhang SN.Hou XL,Yang YG (2007)Studies on ance.Plant Physiol 151:241-252 biochemical characteristics of PolCMS line and its maintainer Piano A,Franzellitti S,Tinti F,Fabbri E (2005)Sequencing and line of Brassica rapa ssp.chinensis.Acta Agriculturae Uni- expression pattern of inducible heat shock gene products in the versitatis Jiangxiensis 4:522-525 European flat oyster,Ostrea edulis.Gene 361:119-126 Erickson L.Grant I.Beversdorf W(1986)Cytoplasmic male sterility in Pratt WB,Toft DO (2003)Regulation of signaling protein function rapeseed (Brassica napus L.).1.Restriction patterns of chloroplast and trafficking by the hsp90/hsp70-based chaperone machinery and mitochondrial DNA.Theor Appl Genet 72:145-150 Exp Biol Med 228:111-133 Fu WD,Shuai L.Yao JT.Yu SH.Liu FL.Duan DL (2010)Molecular Rolland-Lagan AG,Bangham JA,Coen E(2003)Growth dynamics cloning and analysis of a cytosolic Hsp70 gene from Enter- underlying petal shape and asymmetry.Nature 422:161-163 omorpha prolifera (Ulvophyceae,Chlorophyta).Plant Mol Biol Roshandel P,Flowers T (2009)The ionic effects of NaCl on Report28:430-437 physiology and gene expression in rice genotypes differing in Haralampidis K,Milioni D,Rigas S,Hatzopoulos P(2002)Combi- salt tolerance.Plant Soil 315:135-147 natorial interaction of cis elements specifies the expression of the Rutherford SL,Lindquist S (1998)Hsp90 as a capacitor for Arabidopsis AtHsp90-I gene.Plant Physiol 129:1138-1149 morphological evolution.Nature 396:336-342 Ishiguro S,Watanabe Y,Ito N,Nonaka H,Takeda N,Sakai T,Kanaya Samakovli D,Thanou A,Valmas C,Hatzopoulos P (2007)Hsp90 H,Okada K (2002)SHEPHERD is the Arabidopsis GRP94 canalizes developmental perturbation.J Exp Bot 58:3513-3524 responsible for the formation of functional CLAVATA proteins. Sambrook J,Fritsch EF,Maniatis T (1989)Molecular cloning:a EMBO2I:898-908 laboratory manual,2nd edn.Cold Spring Harbor Laboratory, Jackson SE.Queitsch C.Toft D (2004)HSP90:from structure to Cold Spring Harbor phenotype.Nat Struct Mol Biol 11:1152-1156 Scarpeci TE,Zanor MI,Valle EM (2008)Investigating the role of Kemble RJ,Barsby TL (1988)Use of protoplast fusion systems to plant heat shock proteins during oxidative stress.Plant Signal study organelle genetics in a commercially important crop. Behav3:856-857 Biochem Cell Biol 66:665-676 Scharf KD,Siddique M,Vierling E(2001)The expanding family of Kotak S,Vierling E,Baumlein H,von Koskull-Doring P(2007)A Arabidopsis thaliana small heat stress proteins and a new family novel transcriptional cascade regulating expression of heat stress of proteins containing a-crystallin domains (Acd proteins).Cell proteins during seed development of Arabidopsis.Plant Cell Stress Chaperones 6:225-237 19:182-195 Segui-Simarro JM,Testillano PS,Risueno MC (2003)Hsp70 and Li FH,Luan W,Zhang CS,Zhang JQ,Wang B,Xie YS,Li SH,Xiang Hsp90 change their expression and subcellular localization after JH (2009)Cloning of cytoplasmic heat shock protein 90 microspore embryogenesis induction in Brassica napus L.J (FcHSP90)from Fenneropenaeus chinensis and its expression Struct Biol 142:379-391 response to heat shock and hypoxia.Cell Stress Chaperones Sheoran IS,Ross ARS,Olson DJH.Sawhney VK(2009)Differential 14:161-172 expression of proteins in the wild type and 7B-1 male-sterile Lin KH,Lin CH,Chan MT,Lo HF(2010)Identification of flooding- mutant anthers of tomato (Solanum lycopersicum):a proteomic response genes in eggplant roots by suppression subtractive analysis.J Proteomics 71:624-636 hybridization.Plant Mol Biol Report 28:212-221 Song HM,Fan PX,Li YX (2009)Overexpression of organellar and Liu D,Zhang X,Cheng Y,Takano T,Liu S (2006)rHsp90 gene cytosolic AtHSP90 in Arabidopsis thaliana impairs plant expression in response to several environmental stresses in rice tolerance to oxidative stress.Plant Mol Biol Report 27:342-349 (Oryza sativa L.).Plant Physiol Biochem 44:380-386 Swindell WR,Huebner M,Weber AP(2007)Transcriptional profiling Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression of Arabidopsis heat shock proteins and transcription factors data using real-time quantitative PCR and the 2-A4CT Method. reveals extensive overlap between heat and non-heat stress Methods 25:402-408 response pathways.BMC Genomics 8:125-140 么Springermitochondria that will result in the cell progressed death during flower development and then the sterility. Acknowledgments This work was supported by 973 Program (2009CB119001-04) and Program for New Century Excellent Talents in University (NCET-07-0439). References Brown MA, Zhu L, Schmidt C, Tucker PW (2007) Hsp90-From signal transduction to cell transformation. Biochem Biophys Res Commun 363:241–246 Cao ZP, Jia ZW, Liu YJ, Wang M, Zhao JF, Zheng J, Wang GY (2009) Constitutive expression of ZmsHSP in Arabidopsis enhances their cytokinin sensitivity. Mol Biol Rep 10:1089–1097 Dafny-Yelin M, Guterman I, Menda N, Ovadis M, Shalit M, Pichersky E, Zamir D, Lewinsohn E, Adam Z, Weiss D, Vainstein A (2005) Flower proteome: changes in protein spectrum during the advanced stages of rose petal development. Planta 222:37–46 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 Deng XH, Zhang SN, Hou XL, Yang YG (2007) Studies on biochemical characteristics of PolCMS line and its maintainer line of Brassica rapa ssp. chinensis. Acta Agriculturae Uni￾versitatis Jiangxiensis 4:522–525 Erickson L, Grant I, Beversdorf W (1986) Cytoplasmic male sterility in rapeseed (Brassica napus L.). 1. Restriction patterns of chloroplast and mitochondrial DNA. Theor Appl Genet 72:145–150 Fu WD, Shuai L, Yao JT, Yu SH, Liu FL, Duan DL (2010) Molecular cloning and analysis of a cytosolic Hsp70 gene from Enter￾omorpha prolifera (Ulvophyceae, Chlorophyta). Plant Mol Biol Report 28:430–437 Haralampidis K, Milioni D, Rigas S, Hatzopoulos P (2002) Combi￾natorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129:1138–1149 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 21:898–908 Jackson SE, Queitsch C, Toft D (2004) HSP90: from structure to phenotype. Nat Struct Mol Biol 11:1152–1156 Kemble RJ, Barsby TL (1988) Use of protoplast fusion systems to study organelle genetics in a commercially important crop. Biochem Cell Biol 66:665–676 Kotak S, Vierling E, Bäumlein H, von Koskull-Döring P (2007) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19:182–195 Li FH, Luan W, Zhang CS, Zhang JQ, Wang B, Xie YS, Li SH, Xiang JH (2009) Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress Chaperones 14:161–172 Lin KH, Lin CH, Chan MT, Lo HF (2010) Identification of flooding￾response genes in eggplant roots by suppression subtractive hybridization. Plant Mol Biol Report 28:212–221 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 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2
ΔΔCT Method. Methods 25:402–408 Magnard JL, Vergne P, Dumas C (1996) Complexity and genetic variability of heat-shock protein expression in isolated maize microspores. Plant Physiol 111:1085–1096 Marino R, Pinto MR, Cotelli F, Lamia CL, De Santis R (1998) The hsp70 protein is involved in the acquisition of gamete self-sterility in the ascidian Ciona intestinalis. Development 125:899–907 Marrs KA, Casey ES, Capitant SA, Bouchard RA, Dietrich PS, Mettler IJ, Sinibaldi RM (1993) Characterization of two maize hsp90 heat shock protein genes and expression during heat shock, embryogenesis and pollen development. Dev Genet 14:27–41 Mery DY, Tzvi T, Alexander V, Zach A (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 Milioni D, Hatzopoulos P (1997) Genomic organization of hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955–961 Muller L, Schaupp A, Walerych D, Wegele H, Buchner J (2004) Hsp90 regulates the activity of wild type p53 under physiological and elevated temperatures. J Biol Chem 279:48846–48854 Pearl LH, Prodromou C (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75:271–294 Perez DE, Hoyer JS, Johnson AI, Moody ZR, Lopez J, Kaplinsky NJ (2008) BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotoler￾ance. Plant Physiol 151:241–252 Piano A, Franzellitti S, Tinti F, Fabbri E (2005) Sequencing and expression pattern of inducible heat shock gene products in the European flat oyster, Ostrea edulis. Gene 361:119–126 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 Rolland-Lagan AG, Bangham JA, Coen E (2003) Growth dynamics underlying petal shape and asymmetry. Nature 422:161–163 Roshandel P, Flowers T (2009) The ionic effects of NaCl on physiology and gene expression in rice genotypes differing in salt tolerance. Plant Soil 315:135–147 Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342 Samakovli D, Thanou A, Valmas C, Hatzopoulos P (2007) Hsp90 canalizes developmental perturbation. J Exp Bot 58:3513–3524 Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning; a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor Scarpeci TE, Zanor MI, Valle EM (2008) Investigating the role of plant heat shock proteins during oxidative stress. Plant Signal Behav 3:856–857 Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225–237 Seguí-Simarro JM, Testillano PS, Risueňo MC (2003) Hsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus L. J Struct Biol 142:379–391 Sheoran IS, Ross ARS, Olson DJH, Sawhney VK (2009) Differential expression of proteins in the wild type and 7B-1 male-sterile mutant anthers of tomato (Solanum lycopersicum): a proteomic analysis. J Proteomics 71:624–636 Song HM, Fan PX, Li YX (2009) Overexpression of organellar and cytosolic AtHSP90 in Arabidopsis thaliana impairs plant tolerance to oxidative stress. Plant Mol Biol Report 27:342–349 Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125–140 Plant Mol Biol Rep (2011) 29:723–732 731