植物SPFH超家族蛋白及其生物学功能研究进展
|
摘要
膜微区(membrane microdomains)是细胞质膜上富含固醇类和鞘脂类的微结构域,大小为10～200 nm,为一种高度动态的结构。膜微区富含多种标记蛋白,例如GPI(glycosylphosphatidylinositol)锚定蛋白和许多膜整合蛋白。其中SPFH超家族蛋白(Stomatin、Prohibitin、Flotillin and Hflk/C)进化保守,并且广泛分布于原核和真核生物中。研究表明SPFH蛋白具有多种重要的生物学功能,参与植物的抗病、抗逆和生长发育等过程,因此受到了越来越多的关注。本文主要介绍了SPFH超家族蛋白的结构及其寡聚化状态,且进一步综述了SPFH超家族蛋白在植物中的研究进展,以期为今后系统开展其在膜微区形成过程中的功能研究提供理论依据。
Membrane microdomains are nano-scale domains( 10-200 nm) enriched in sterols and sphingolipids. They are small and highly dynamic to host glycosylphosphatidylinositol( GPI)-anchored proteins and a subset of cell surface proteins. Among them,the SPFH domain-containing proteins( Stomatin,Prohibitin,Flotillin and HIR) are evolutionary conserved and present in both prokaryotes and eukaryotes. Recently,more and more evidences support the conclusion that SPFH superfamily proteins play important roles in response to biotic and abiotic stresses. Therefore,this review focuses on the structures and oligomerization of SPFH domain family proteins,with special emphasis on recent progresses in biological functions of these proteins in plants,which will provide valuable information for further studies on SPFH proteins in the formation of membrane microdomains.
Membrane microdomains are nano-scale domains( 10-200 nm) enriched in sterols and sphingolipids. They are small and highly dynamic to host glycosylphosphatidylinositol( GPI)-anchored proteins and a subset of cell surface proteins. Among them,the SPFH domain-containing proteins( Stomatin,Prohibitin,Flotillin and HIR) are evolutionary conserved and present in both prokaryotes and eukaryotes. Recently,more and more evidences support the conclusion that SPFH superfamily proteins play important roles in response to biotic and abiotic stresses. Therefore,this review focuses on the structures and oligomerization of SPFH domain family proteins,with special emphasis on recent progresses in biological functions of these proteins in plants,which will provide valuable information for further studies on SPFH proteins in the formation of membrane microdomains.
引文
[1]崔亚宁,李晓娟,林金星,等.脂筏及其在植物细胞中的研究进展[J].电子显微学报,2014,33(5):469-477.
[2] SINGER S J,NICOLSON G L. The fluid mosaic model of the structure of cell membranes[J]. Science,1972,175(4023):720-731.
[3] SIMONS K, IKONEN E. Functional rafts in cell membranes[J]. Nature,1997,387(6633):569-572.
[4] JACOBSON K,MOURITSEN O G,ANDERSON R G.Lipid rafts:at a crossroad between cell biology and physics[J]. Nat Cell Biol,2007,9(1):7-14.
[5]玉猛,吕雪芹,林金星,等.植物脂筏微区参与病原菌的防御反应[J].电子显微学报,2016,35(2):163-170.
[6] MORROW I C,PARTON R G. Flotillins and the PHB domain protein family:rafts,worms and anaesthetics[J]. Traffic,2005,6(9):725-740.
[7] RIVERA-MILLA E, STUERMER C A, MALAGATRILLO E. Ancient origin of reggie(flotillin),reggielike,and other lipid-raft proteins:convergent evolution of the SPFH domain[J]. Cell Mol Life Sci,2006,63(3):343-357.
[8] NADIMPALLI R,YALPANI N,JOHAL G S,et al.Prohibitins,stomatins,and plant disease response genes compose a protein superfamily that controls cell proliferation,ion channel regulation,and death[J]. J Biol Chem,2000,275(38):29579-29586.
[9] CHOI H W, KIM Y J, HWANG B K. The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity[J]. Mol Plant Microbe Interact,2011,24(1):68-78.
[10] BROWMAN D T,RESEK M E,ZAJCHOWSKI L D,et al. Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER[J]. J Cell Sci,2006,119(Pt 15):3149-3160.
[11] WETZEL C, HU J, RIETHMACHER D, et al. A stomatin-domain protein essential for touch sensation in the mouse[J]. Nature,2007,445(7124):206-209.
[12] LANGHORST M F,REUTER A,STUERMER C A.Scaffolding microdomains and beyond:the function of reggie/flotillin proteins[J]. Cell Mol Life Sci,2005,62(19/20):2228-2240.
[13] HUBER T B,SCHERMER B,MULLER R U,et al.Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels[J]. Proc Natl Acad Sci U S A,2006,103(46):17079-17086.
[14] BROWMAN D T,HOEGG M B,ROBBINS S M. The SPFH domain-containing proteins:more than lipid raft markers[J]. Trends Cell Biol,2007,17(8):394-402.
[15] TATSUTA T,MODEL K,LANGER T. Formation of membrane-bound ring complexes by prohibitins in mitochondria[J]. Mol Biol Cell,2005,16(1):248-259.
[16] QI Y,TSUDA K,GLAZEBROOK J,et al. Physical association of pattern-triggered immunity(PTI)and effector-triggered immunity(ETI)immune receptors in Arabidopsis[J]. Mol Plant Pathol,2011,12(7):702-708.
[17] QI Y,KATAGIRI F. Membrane microdomain may be a platform for immune signaling[J]. Plant Signal Behav,2012,7(4):454-456.
[18] SABHARANJAK S,SHARMA P,PARTON R G,et al.GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrinindependent pinocytic pathway[J]. Dev Cell,2002,2(4):411-423.
[19] KIRKHAM M, FUJITA A, CHADDA R, et al.Ultrastructural identification of uncoated caveolinindependent early endocytic vehicles[J]. J Cell Biol,2005,168(3):465-476.
[20] ROTH T F,PORTER K R. Yolk protein uptake in the oocyte of the mosquito Aedes aegypti.L[J]. J Cell Biol,1964,20:313-332.
[21] PARTON R G, SIMONS K. The multiple faces of caveolae[J]. Nat Rev Mol Cell Biol,2007,8(3):185-194.
[22] BAUER M, PELKMANS L. A new paradigm for membrane-organizing and-shaping scaffolds[J]. FEBS Lett,2006,580(23):5559-5564.
[23] ANDERSON R G,JACOBSON K. A role for lipid shells in targeting proteins to caveolae,rafts,and other lipid domains[J]. Science,2002,296(5574):1821-1825.
[24] HUBER T B,BENZING T. The slit diaphragm:a signaling platform to regulate podocyte function[J]. Curr Opin Nephrol Hypertens,2005,14(3):211-216.
[25] MISHRA S,MURPHY L C,NYOMBA B L,et al.Prohibitin:a potential target for new therapeutics[J].Trends Mol Med,2005,11(4):192-197.
[26] GEHL B. Functional and molecular characterisation of two stomatin-like proteins from Arabidopsis thaliana[D]. UK:University of Glasgow,2009.
[27] CHRISTIANS M J,LARSEN P B. Mutational loss of the prohibitin At PHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings[J]. J Exp Bot,2007,58(8):2237-2248.
[28] Van AKEN O,PECENKOVA T,Van De COTTE B,et al. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development[J]. Plant J,2007,52(5):850-864.
[29] KONG X,TIAN H,YU Q,et al. PHB3 maintains root stem cell niche identity through ROS-Responsive AP2/ERF transcription factors in Arabidopsis[J]. Cell Rep,2018,22(5):1350-1363.
[30] WANG Y,RIES A,WU K,et al. The Arabidopsis Prohibitin Gene PHB3 functions in nitric oxide-mediated responses and in hydrogen peroxide-induced nitric oxide accumulation[J]. Plant Cell,2010,22(1):249-259.
[31] PIECHOTA J,BEREZA M,SOKOLOWSKA A,et al.Unraveling the functions of type II-prohibitins in Arabidopsis mitochondria[J]. Plant Mol Biol,2015,88(3):249-267.
[32] MOGK A, HASLBERGER T, TESSARZ P, et al.Common and specific mechanisms of AAA+proteins involved in protein quality control[J]. Biochem Soc Trans,2008,36(Pt 1):120-125.
[33] AHN C S, LEE J H, REUM HWANG A, et al.Prohibitin is involved in mitochondrial biogenesis in plants[J]. Plant J,2006,46(4):658-667.
[34] TAKAHASHI A,KAWASAKI T,WONG H L,et al.Hyperphosphorylation of a mitochondrial protein,prohibitin,is induced by calyculin A in a rice lesionmimic mutant cdr1[J]. Plant Physiol,2003,132(4):1861-1869.
[35] CHEN F,YUAN Y,LI Q,et al. Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight[J]. Proteomics,2007,7(9):1529-1539.
[36] LI R,LIU P,WAN Y,et al. A membrane microdomain-associated protein,Arabidopsis Flot1,is involved in a clathrin-independent endocytic pathway and is required for seedling development[J]. Plant Cell,2012,24(5):2105-2122.
[37] MENG YU,HAIJIAO LIU,ZIYI DONG,et al. The dynamics and endocytosis of Flot1 protein in response to flg22 in Arabidopsis[J]. J Plant Physiol,2017,215:73-84.
[38] HANEY C H,LONG S R. Plant flotillins are required for infection by nitrogen-fixing bacteria[J]. Proc Natl Acad Sci USA,2010,107(1):478-483.
[39] JUNG H W,HWANG B K. The leucine-rich repeat(LRR)protein, Ca LRR1, interacts with the hypersensitive induced reaction(HIR)protein,Ca HIR1,and suppresses cell death induced by the Ca HIR1 protein[J]. Mol Plant Pathol,2007,8(4):503-514.
[40] ZHOU L,CHEUNG M Y,ZHANG Q,et al. A novel simple extracellular leucine-rich repeat(e LRR)domain protein from rice(Os LRR1)enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1(Os HIR1)[J]. Plant Cell Environ,2009,32(12):1804-1820.
[41] QI Y,TSUDA K,NGUYEN LE V,et al. Physical association of Arabidopsis hypersensitive induced reaction proteins(HIRs)with the immune receptor RPS2[J]. J Biol Chem,2011,286(36):31297-31307.
[42] DUAN Y,GUO J,SHI X,et al. Wheat hypersensitiveinduced reaction genes Ta HIR1 and Ta HIR3 are involved in response to stripe rust fungus infection and abiotic stresses[J]. Plant Cell Rep,2013,32(2):273-283.
[43] FEN LIU X Y,WEIQUAN ZHAO,JIAPING CHEN,et al. Effects of the leaf rust pathogen on expression of Ta HIR4 at the gene and protein levels in wheat[J].Journal of Plant Interactions,2013,8(4):304-311.
[44] HIEBL-DIRSCHMIED C M,ADOLF G R,PROHASKA R. Isolation and partial characterization of the human erythrocyte band 7 integral membrane protein[J].Biochim Biophys Acta,1991,1065(2):195-202.
[45] SNYERS L,THINES-SEMPOUX D,PROHASKA R.Colocalization of stomatin(band 7. 2b)and actin microfilaments in UAC epithelial cells[J]. Eur J Cell Biol,1997,73(3):281-285.
[46] SNYERS L,UMLAUF E,PROHASKA R. Association of stomatin with lipid-protein complexes in the plasma membrane and the endocytic compartment[J]. Eur J Cell Biol,1999,78(11):802-812.
[47] BRAND J,SMITH E S,SCHWEFEL D,et al. A stomatin dimer modulates the activity of acid-sensing ion channels[J]. EMBO J,2012,31(17):3635-3646.
[48] MITSOPOULOS P,LAPOHOS O,WERAARPACHAI W,et al. Stomatin-like protein 2 deficiency results in impaired mitochondrial translation[J]. PLoS One,2017,12(6):e0179967.
[49] BARTOLOME A,BOSKOVIC S,PAUNOVIC I,et al.Stomatin-like protein 2 overexpression in papillary thyroid carcinoma is significantly associated with highrisk clinicopathological parameters and BRAFV600E mutation[J]. APMIS,2016,124(4):271-277.
[50] CHEN C Y,YANG C Y,CHEN Y C,et al. Decreased expression of stomatin predicts poor prognosis in HER2-positive breast cancer[J]. Bmc Cancer,2016,16:697.
[51] FENG Q,HU Z Y,LIU X Q,et al. Stomatin-like protein 2 is involved in endometrial stromal cell proliferation and differentiation during decidualization in mice and humans[J]. Reprod Biomed Online,2017,34(2):191-202.
[52] HEAZLEWOOD J L,TONTI-FILIPPINI J S,GOUT A M, et al. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components,provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins[J]. Plant Cell,2004,16(1):241-256.
[53] BORNER G H,SHERRIER D J,WEIMAR T,et al.Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts[J]. Plant Physiol,2005,137(1):104-116.
[54] DUNKLEY T P,HESTER S,SHADFORTH I P,et al.Mapping the Arabidopsis organelle proteome[J]. Proc Natl Acad Sci USA,2006,103(17):6518-6523.
[55] MITRA S K,GANTT J A,RUBY J F,et al. Membrane proteomic analysis of Arabidopsis thaliana using alternative solubilization techniques[J]. J Proteome Res,2007,6(5):1933-1950.
[56] GEHL B,LEE C P,BOTA P,et al. An Arabidopsis stomatin-like protein affects mitochondrial respiratory supercomplex organization[J]. Plant Physiol,2014,164(3):1389-1400.
[57] TAIZ L,ZEIGER E. Respiration and lipid metabolism[J]. In Plant Physiology,2002:223-258.
[58] MOLLER I M. Plant mitochondria and oxidative stress:electron transport,NADPH turnover,and metabolism of reactive oxygen species[J]. Annu Rev Plant Physiol Plant Mol Biol,2001,52:561-591.
[59] LOGAN D C,MILLAR A H,SWEETLOVE L J,et al.Mitochondrial biogenesis during germination in maize embryos[J]. Plant Physiol,2001,125(2):662-672.
[60] DELL'ORCO R T,MCCLUNG J K,JUPE E R,et al.Prohibitin and the senescent phenotype[J]. Exp Gerontol,1996,31(1/2):245-252.
[61] COATES P J,JAMIESON D J,SMART K,et al. The prohibitin family of mitochondrial proteins regulate replicative lifespan[J]. Curr Biol,1997,7(8):607-610.
[62] WELBURN S C,MURPHY N B. Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms[J]. Cell Death Differ,1998,5(7):615-622.
[63] IKONEN E, FIEDLER K, PARTON R G, et al.Prohibitin,an antiproliferative protein,is localized to mitochondria[J]. FEBS Lett,1995,358(3):273-277.
[64] SNEDDEN W A,FROMM H. Characterization of the plant homologue of prohibitin,a gene associated with antiproliferative activity in mammalian cells[J]. Plant Mol Biol,1997,33(4):753-756.
[65] NIJTMANS L G,DE JONG L,ARTAL SANZ M,et al.Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins[J]. EMBO J,2000,19(11):2444-2451.
[66] STEGLICH G,NEUPERT W,LANGER T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria[J]. Mol Cell Biol,1999,19(5):3435-3442.
[67] KRUFT V,EUBEL H,JANSCH L,et al. Proteomic approach to identify novel mitochondrial proteins in Arabidopsis[J]. Plant Physiol,2001,127(4):1694-1710.
[68] MILLAR A H,SWEETLOVE L J,GIEGE P,et al.Analysis of the Arabidopsis mitochondrial proteome[J].Plant Physiol,2001,127(4):1711-1727.
[69] CHEN J C,JIANG C Z,REID M S. Silencing a prohibitin alters plant development and senescence[J].Plant J,2005,44(1):16-24.
[70] SONG J,CHEN W,LU Z,et al. Soluble expression,purification,and characterization of recombinant human flotillin-2(reggie-1)in Escherichia coli[J]. Mol Biol Rep,2011,38(3):2091-2098.
[71] TAVERNARAKIS N,DRISCOLL M,KYRPIDES N C.The SPFH domain:implicated in regulating targeted protein turnover in stomatins and other membraneassociated proteins[J]. Trends Biochem Sci,1999,24(11):425-427.
[72] NEUMANN-GIESEN C,FALKENBACH B,BEICHT P,et al. Membrane and raft association of reggie-1/flotillin-2:role of myristoylation,palmitoylation and oligomerization and induction of filopodia by overexpression[J]. Biochem J,2004,378(Pt 2):509-518.
[73] SOLIS G P,HOEGG M,MUNDERLOH C,et al.Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains[J]. Biochem J,2007,403(2):313-322.
[74] MATSUMURA H,NIRASAWA S, KIBA A, et al.Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice(Oryza sativa L)cells[J]. Plant J,2003,33(3):425-434.
[75] KAWAI-YAMADA M, OHORI Y, UCHIMIYA H.Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-,hydrogen peroxide-,and salicylic acid-induced cell death[J]. Plant Cell,2004,16(1):21-32.
[76] ISHIKAWA T, AKI T, YANAGISAWA S, et al.Overexpression of BAX INHIBITOR-1 links plasma membrane microdomain proteins to stress[J]. Plant Physiol,2015,169(2):1333-1343.
[77] JUNG H W,LIM C W,LEE S C,et al. Distinct roles of the pepper hypersensitive induced reaction protein gene Ca HIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses[J]. Planta,2008,227(2):409-425.
[78] CHOI H W,KIM D S,KIM N H,et al. Xanthomonas filamentous hemagglutinin-like protein Fha1 interacts with pepper hypersensitive-induced reaction protein Ca HIR1 and functions as a virulence factor in host plants[J]. Mol Plant Microbe Interact,2013,26(12):1441-1454.
[79] ZHOU L, CHEUNG M Y, LI M W, et al. Rice hypersensitive induced reaction protein 1(Os HIR1)associates with plasma membrane and triggers hypersensitive cell death[J]. BMC Plant Biol,2010,10:290.
[80] MOLINA A,GORLACH J,VOLRATH S,et al. Wheat genes encoding two types of PR-1 proteins are pathogen inducible,but do not respond to activators of systemic acquired resistance[J]. Mol Plant Microbe Interact,1999,12(1):53-58.
[81] LU Z X,GAUDET D,PUCHALSKI B,et al. Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression[J]. Physiol Mol Plant Pathol,2006,67(3):138-148.
[82] NIU J,LIU R,ZHENG L. Expression analysis of wheat PR-1,PR-2,PR-5 activated by Bgt and SA,and powdery mildew resistance[J]. J Triticeae Crops,2007,27:1132-1137.
[2] SINGER S J,NICOLSON G L. The fluid mosaic model of the structure of cell membranes[J]. Science,1972,175(4023):720-731.
[3] SIMONS K, IKONEN E. Functional rafts in cell membranes[J]. Nature,1997,387(6633):569-572.
[4] JACOBSON K,MOURITSEN O G,ANDERSON R G.Lipid rafts:at a crossroad between cell biology and physics[J]. Nat Cell Biol,2007,9(1):7-14.
[5]玉猛,吕雪芹,林金星,等.植物脂筏微区参与病原菌的防御反应[J].电子显微学报,2016,35(2):163-170.
[6] MORROW I C,PARTON R G. Flotillins and the PHB domain protein family:rafts,worms and anaesthetics[J]. Traffic,2005,6(9):725-740.
[7] RIVERA-MILLA E, STUERMER C A, MALAGATRILLO E. Ancient origin of reggie(flotillin),reggielike,and other lipid-raft proteins:convergent evolution of the SPFH domain[J]. Cell Mol Life Sci,2006,63(3):343-357.
[8] NADIMPALLI R,YALPANI N,JOHAL G S,et al.Prohibitins,stomatins,and plant disease response genes compose a protein superfamily that controls cell proliferation,ion channel regulation,and death[J]. J Biol Chem,2000,275(38):29579-29586.
[9] CHOI H W, KIM Y J, HWANG B K. The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity[J]. Mol Plant Microbe Interact,2011,24(1):68-78.
[10] BROWMAN D T,RESEK M E,ZAJCHOWSKI L D,et al. Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER[J]. J Cell Sci,2006,119(Pt 15):3149-3160.
[11] WETZEL C, HU J, RIETHMACHER D, et al. A stomatin-domain protein essential for touch sensation in the mouse[J]. Nature,2007,445(7124):206-209.
[12] LANGHORST M F,REUTER A,STUERMER C A.Scaffolding microdomains and beyond:the function of reggie/flotillin proteins[J]. Cell Mol Life Sci,2005,62(19/20):2228-2240.
[13] HUBER T B,SCHERMER B,MULLER R U,et al.Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels[J]. Proc Natl Acad Sci U S A,2006,103(46):17079-17086.
[14] BROWMAN D T,HOEGG M B,ROBBINS S M. The SPFH domain-containing proteins:more than lipid raft markers[J]. Trends Cell Biol,2007,17(8):394-402.
[15] TATSUTA T,MODEL K,LANGER T. Formation of membrane-bound ring complexes by prohibitins in mitochondria[J]. Mol Biol Cell,2005,16(1):248-259.
[16] QI Y,TSUDA K,GLAZEBROOK J,et al. Physical association of pattern-triggered immunity(PTI)and effector-triggered immunity(ETI)immune receptors in Arabidopsis[J]. Mol Plant Pathol,2011,12(7):702-708.
[17] QI Y,KATAGIRI F. Membrane microdomain may be a platform for immune signaling[J]. Plant Signal Behav,2012,7(4):454-456.
[18] SABHARANJAK S,SHARMA P,PARTON R G,et al.GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrinindependent pinocytic pathway[J]. Dev Cell,2002,2(4):411-423.
[19] KIRKHAM M, FUJITA A, CHADDA R, et al.Ultrastructural identification of uncoated caveolinindependent early endocytic vehicles[J]. J Cell Biol,2005,168(3):465-476.
[20] ROTH T F,PORTER K R. Yolk protein uptake in the oocyte of the mosquito Aedes aegypti.L[J]. J Cell Biol,1964,20:313-332.
[21] PARTON R G, SIMONS K. The multiple faces of caveolae[J]. Nat Rev Mol Cell Biol,2007,8(3):185-194.
[22] BAUER M, PELKMANS L. A new paradigm for membrane-organizing and-shaping scaffolds[J]. FEBS Lett,2006,580(23):5559-5564.
[23] ANDERSON R G,JACOBSON K. A role for lipid shells in targeting proteins to caveolae,rafts,and other lipid domains[J]. Science,2002,296(5574):1821-1825.
[24] HUBER T B,BENZING T. The slit diaphragm:a signaling platform to regulate podocyte function[J]. Curr Opin Nephrol Hypertens,2005,14(3):211-216.
[25] MISHRA S,MURPHY L C,NYOMBA B L,et al.Prohibitin:a potential target for new therapeutics[J].Trends Mol Med,2005,11(4):192-197.
[26] GEHL B. Functional and molecular characterisation of two stomatin-like proteins from Arabidopsis thaliana[D]. UK:University of Glasgow,2009.
[27] CHRISTIANS M J,LARSEN P B. Mutational loss of the prohibitin At PHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings[J]. J Exp Bot,2007,58(8):2237-2248.
[28] Van AKEN O,PECENKOVA T,Van De COTTE B,et al. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development[J]. Plant J,2007,52(5):850-864.
[29] KONG X,TIAN H,YU Q,et al. PHB3 maintains root stem cell niche identity through ROS-Responsive AP2/ERF transcription factors in Arabidopsis[J]. Cell Rep,2018,22(5):1350-1363.
[30] WANG Y,RIES A,WU K,et al. The Arabidopsis Prohibitin Gene PHB3 functions in nitric oxide-mediated responses and in hydrogen peroxide-induced nitric oxide accumulation[J]. Plant Cell,2010,22(1):249-259.
[31] PIECHOTA J,BEREZA M,SOKOLOWSKA A,et al.Unraveling the functions of type II-prohibitins in Arabidopsis mitochondria[J]. Plant Mol Biol,2015,88(3):249-267.
[32] MOGK A, HASLBERGER T, TESSARZ P, et al.Common and specific mechanisms of AAA+proteins involved in protein quality control[J]. Biochem Soc Trans,2008,36(Pt 1):120-125.
[33] AHN C S, LEE J H, REUM HWANG A, et al.Prohibitin is involved in mitochondrial biogenesis in plants[J]. Plant J,2006,46(4):658-667.
[34] TAKAHASHI A,KAWASAKI T,WONG H L,et al.Hyperphosphorylation of a mitochondrial protein,prohibitin,is induced by calyculin A in a rice lesionmimic mutant cdr1[J]. Plant Physiol,2003,132(4):1861-1869.
[35] CHEN F,YUAN Y,LI Q,et al. Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight[J]. Proteomics,2007,7(9):1529-1539.
[36] LI R,LIU P,WAN Y,et al. A membrane microdomain-associated protein,Arabidopsis Flot1,is involved in a clathrin-independent endocytic pathway and is required for seedling development[J]. Plant Cell,2012,24(5):2105-2122.
[37] MENG YU,HAIJIAO LIU,ZIYI DONG,et al. The dynamics and endocytosis of Flot1 protein in response to flg22 in Arabidopsis[J]. J Plant Physiol,2017,215:73-84.
[38] HANEY C H,LONG S R. Plant flotillins are required for infection by nitrogen-fixing bacteria[J]. Proc Natl Acad Sci USA,2010,107(1):478-483.
[39] JUNG H W,HWANG B K. The leucine-rich repeat(LRR)protein, Ca LRR1, interacts with the hypersensitive induced reaction(HIR)protein,Ca HIR1,and suppresses cell death induced by the Ca HIR1 protein[J]. Mol Plant Pathol,2007,8(4):503-514.
[40] ZHOU L,CHEUNG M Y,ZHANG Q,et al. A novel simple extracellular leucine-rich repeat(e LRR)domain protein from rice(Os LRR1)enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1(Os HIR1)[J]. Plant Cell Environ,2009,32(12):1804-1820.
[41] QI Y,TSUDA K,NGUYEN LE V,et al. Physical association of Arabidopsis hypersensitive induced reaction proteins(HIRs)with the immune receptor RPS2[J]. J Biol Chem,2011,286(36):31297-31307.
[42] DUAN Y,GUO J,SHI X,et al. Wheat hypersensitiveinduced reaction genes Ta HIR1 and Ta HIR3 are involved in response to stripe rust fungus infection and abiotic stresses[J]. Plant Cell Rep,2013,32(2):273-283.
[43] FEN LIU X Y,WEIQUAN ZHAO,JIAPING CHEN,et al. Effects of the leaf rust pathogen on expression of Ta HIR4 at the gene and protein levels in wheat[J].Journal of Plant Interactions,2013,8(4):304-311.
[44] HIEBL-DIRSCHMIED C M,ADOLF G R,PROHASKA R. Isolation and partial characterization of the human erythrocyte band 7 integral membrane protein[J].Biochim Biophys Acta,1991,1065(2):195-202.
[45] SNYERS L,THINES-SEMPOUX D,PROHASKA R.Colocalization of stomatin(band 7. 2b)and actin microfilaments in UAC epithelial cells[J]. Eur J Cell Biol,1997,73(3):281-285.
[46] SNYERS L,UMLAUF E,PROHASKA R. Association of stomatin with lipid-protein complexes in the plasma membrane and the endocytic compartment[J]. Eur J Cell Biol,1999,78(11):802-812.
[47] BRAND J,SMITH E S,SCHWEFEL D,et al. A stomatin dimer modulates the activity of acid-sensing ion channels[J]. EMBO J,2012,31(17):3635-3646.
[48] MITSOPOULOS P,LAPOHOS O,WERAARPACHAI W,et al. Stomatin-like protein 2 deficiency results in impaired mitochondrial translation[J]. PLoS One,2017,12(6):e0179967.
[49] BARTOLOME A,BOSKOVIC S,PAUNOVIC I,et al.Stomatin-like protein 2 overexpression in papillary thyroid carcinoma is significantly associated with highrisk clinicopathological parameters and BRAFV600E mutation[J]. APMIS,2016,124(4):271-277.
[50] CHEN C Y,YANG C Y,CHEN Y C,et al. Decreased expression of stomatin predicts poor prognosis in HER2-positive breast cancer[J]. Bmc Cancer,2016,16:697.
[51] FENG Q,HU Z Y,LIU X Q,et al. Stomatin-like protein 2 is involved in endometrial stromal cell proliferation and differentiation during decidualization in mice and humans[J]. Reprod Biomed Online,2017,34(2):191-202.
[52] HEAZLEWOOD J L,TONTI-FILIPPINI J S,GOUT A M, et al. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components,provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins[J]. Plant Cell,2004,16(1):241-256.
[53] BORNER G H,SHERRIER D J,WEIMAR T,et al.Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts[J]. Plant Physiol,2005,137(1):104-116.
[54] DUNKLEY T P,HESTER S,SHADFORTH I P,et al.Mapping the Arabidopsis organelle proteome[J]. Proc Natl Acad Sci USA,2006,103(17):6518-6523.
[55] MITRA S K,GANTT J A,RUBY J F,et al. Membrane proteomic analysis of Arabidopsis thaliana using alternative solubilization techniques[J]. J Proteome Res,2007,6(5):1933-1950.
[56] GEHL B,LEE C P,BOTA P,et al. An Arabidopsis stomatin-like protein affects mitochondrial respiratory supercomplex organization[J]. Plant Physiol,2014,164(3):1389-1400.
[57] TAIZ L,ZEIGER E. Respiration and lipid metabolism[J]. In Plant Physiology,2002:223-258.
[58] MOLLER I M. Plant mitochondria and oxidative stress:electron transport,NADPH turnover,and metabolism of reactive oxygen species[J]. Annu Rev Plant Physiol Plant Mol Biol,2001,52:561-591.
[59] LOGAN D C,MILLAR A H,SWEETLOVE L J,et al.Mitochondrial biogenesis during germination in maize embryos[J]. Plant Physiol,2001,125(2):662-672.
[60] DELL'ORCO R T,MCCLUNG J K,JUPE E R,et al.Prohibitin and the senescent phenotype[J]. Exp Gerontol,1996,31(1/2):245-252.
[61] COATES P J,JAMIESON D J,SMART K,et al. The prohibitin family of mitochondrial proteins regulate replicative lifespan[J]. Curr Biol,1997,7(8):607-610.
[62] WELBURN S C,MURPHY N B. Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms[J]. Cell Death Differ,1998,5(7):615-622.
[63] IKONEN E, FIEDLER K, PARTON R G, et al.Prohibitin,an antiproliferative protein,is localized to mitochondria[J]. FEBS Lett,1995,358(3):273-277.
[64] SNEDDEN W A,FROMM H. Characterization of the plant homologue of prohibitin,a gene associated with antiproliferative activity in mammalian cells[J]. Plant Mol Biol,1997,33(4):753-756.
[65] NIJTMANS L G,DE JONG L,ARTAL SANZ M,et al.Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins[J]. EMBO J,2000,19(11):2444-2451.
[66] STEGLICH G,NEUPERT W,LANGER T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria[J]. Mol Cell Biol,1999,19(5):3435-3442.
[67] KRUFT V,EUBEL H,JANSCH L,et al. Proteomic approach to identify novel mitochondrial proteins in Arabidopsis[J]. Plant Physiol,2001,127(4):1694-1710.
[68] MILLAR A H,SWEETLOVE L J,GIEGE P,et al.Analysis of the Arabidopsis mitochondrial proteome[J].Plant Physiol,2001,127(4):1711-1727.
[69] CHEN J C,JIANG C Z,REID M S. Silencing a prohibitin alters plant development and senescence[J].Plant J,2005,44(1):16-24.
[70] SONG J,CHEN W,LU Z,et al. Soluble expression,purification,and characterization of recombinant human flotillin-2(reggie-1)in Escherichia coli[J]. Mol Biol Rep,2011,38(3):2091-2098.
[71] TAVERNARAKIS N,DRISCOLL M,KYRPIDES N C.The SPFH domain:implicated in regulating targeted protein turnover in stomatins and other membraneassociated proteins[J]. Trends Biochem Sci,1999,24(11):425-427.
[72] NEUMANN-GIESEN C,FALKENBACH B,BEICHT P,et al. Membrane and raft association of reggie-1/flotillin-2:role of myristoylation,palmitoylation and oligomerization and induction of filopodia by overexpression[J]. Biochem J,2004,378(Pt 2):509-518.
[73] SOLIS G P,HOEGG M,MUNDERLOH C,et al.Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains[J]. Biochem J,2007,403(2):313-322.
[74] MATSUMURA H,NIRASAWA S, KIBA A, et al.Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice(Oryza sativa L)cells[J]. Plant J,2003,33(3):425-434.
[75] KAWAI-YAMADA M, OHORI Y, UCHIMIYA H.Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-,hydrogen peroxide-,and salicylic acid-induced cell death[J]. Plant Cell,2004,16(1):21-32.
[76] ISHIKAWA T, AKI T, YANAGISAWA S, et al.Overexpression of BAX INHIBITOR-1 links plasma membrane microdomain proteins to stress[J]. Plant Physiol,2015,169(2):1333-1343.
[77] JUNG H W,LIM C W,LEE S C,et al. Distinct roles of the pepper hypersensitive induced reaction protein gene Ca HIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses[J]. Planta,2008,227(2):409-425.
[78] CHOI H W,KIM D S,KIM N H,et al. Xanthomonas filamentous hemagglutinin-like protein Fha1 interacts with pepper hypersensitive-induced reaction protein Ca HIR1 and functions as a virulence factor in host plants[J]. Mol Plant Microbe Interact,2013,26(12):1441-1454.
[79] ZHOU L, CHEUNG M Y, LI M W, et al. Rice hypersensitive induced reaction protein 1(Os HIR1)associates with plasma membrane and triggers hypersensitive cell death[J]. BMC Plant Biol,2010,10:290.
[80] MOLINA A,GORLACH J,VOLRATH S,et al. Wheat genes encoding two types of PR-1 proteins are pathogen inducible,but do not respond to activators of systemic acquired resistance[J]. Mol Plant Microbe Interact,1999,12(1):53-58.
[81] LU Z X,GAUDET D,PUCHALSKI B,et al. Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression[J]. Physiol Mol Plant Pathol,2006,67(3):138-148.
[82] NIU J,LIU R,ZHENG L. Expression analysis of wheat PR-1,PR-2,PR-5 activated by Bgt and SA,and powdery mildew resistance[J]. J Triticeae Crops,2007,27:1132-1137.