植物病原物效应子与寄主植物互作的研究进展
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摘要
植物病原物在侵染寄主过程中会分泌与寄主植物相互作用的蛋白,这类蛋白称为效应蛋白(效应子),这些效应蛋白在植物细胞内发挥着重要作用,从而影响植物病原物与寄主的相互作用。针对植物病原物效应子功能及其作用机理的研究将有助于更好地了解植物病原物与寄主植物相互作用的分子机制。本研究对细菌、卵菌、真菌和线虫的效应子的研究进展进行了综述,并重点阐述了这4类病原物与寄主植物相互作用的理论基础、效应子的功能机制,这些研究结果可为未来作物抗病改良和病害防控策略的制定提供参考。
Plant pathogens will secrete proteins that can interact with host plants during the process of infecting hosts, and these proteins are called effector proteins, which play important roles in plant cells and thus affect the interaction between plant pathogens and their hosts. Researches on the functions and their mechanisms of plant pathogen effectors will be helpful to better understand the molecular mechanisms of the interactions between plant pathogens and their host plants. In this paper, the progress of the study on the effectors of bacteria, oomycetes,fungi and nematodes was reviewed, and the emphasis was focused on the theoretical basis of the interactions between these four pathogens and their host plants as well as the functional mechanisms of the effectors, and these findings could provide a reference for the future crop improvement and disease control strategies.
Plant pathogens will secrete proteins that can interact with host plants during the process of infecting hosts, and these proteins are called effector proteins, which play important roles in plant cells and thus affect the interaction between plant pathogens and their hosts. Researches on the functions and their mechanisms of plant pathogen effectors will be helpful to better understand the molecular mechanisms of the interactions between plant pathogens and their host plants. In this paper, the progress of the study on the effectors of bacteria, oomycetes,fungi and nematodes was reviewed, and the emphasis was focused on the theoretical basis of the interactions between these four pathogens and their host plants as well as the functional mechanisms of the effectors, and these findings could provide a reference for the future crop improvement and disease control strategies.
引文
Alfano J.R.,and Collmer A.,2004,TypeⅢsecretion system effector proteins:double agents in bacterial disease and plant defense,Annu.Rev.Phytopathol.,42:385-414
Anderson J.P.,Gleason C.A.,Foley R.C.,Thrall P.H.,Burdon JB.,and Singh K.B.,2010,Plants versus pathogens:an evolutionary arms race,Functional Plant Biology,37(6)499-512
Chen J.S.,Lin B.R.,Huang Q.L.,Hu L.L.,Zhuo K.,and Liao J.L.2017,A novel Meloidogyne graminicola effector,Mg GPP,is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism,PLo S Pathogens,13(4):e1006301
Chen Q.G.,Shu C.W.,Yang M.,and Zhou E.X.,2016,Research advance on the effectors of plant pathogenic fungi,Jiyinzuxue Yu Yingyong Shengwuxue(Genomics and Applied Biology)35(11):3105-3114(陈琦光,舒灿伟,杨媚,周而勋,2016植物病原真菌效应分子的研究进展,基因组学与应用生物学,35(11):3105-3114)
Chen Q.G.,Wangchen J.Z.,Yang M.,and Zhou E.X.,2015Prediction of candidate effectors from the genome of Colletotrichum higginsianum,Redai Zuowu Xuebao(Chinese Journal of Tropical Crops),36(6):1105-1111(陈琦光,王陈骄子,杨媚,周而勋,2015,希金斯刺盘孢全基因组候选效应分子的预测,热带作物学报,36(6):1105-1111)
Dangl J.L.,and Jones J.D.,2001,Plant pathogens and integrated defence responses to infection,Nature,411(6839):826-833
Davis E.L.,Hussey R.S.,Baum T.J.,Bakker J.,Schots A.,Rosso M.N.,and Abad P.,2000,Nematode:parasitism genes Annu.Rev.Phytopathol.,38(4):365-396
Davis E.L.,Hussey R.S.,Mitchum M.G.,and Baum T.J.,2008Parasitism proteins in nematode-plant interactions,Curr Opin.Plant Biol.,11(4):360-366
De Jonge R.,Van Esse H.P.,Kombrink A.,Shinya T.,Desaki Y.Bours R.,Van der Krol S.,Shibuya N.,Joosten M.H.,and Thomma B.P.,2010,Conserved fungal Lys M effector Ecp6prevents chitin-triggered immunity in plants,Science,329(5994):953-955
Dou D.L.,Kale S.D.,Wang X.L.,Chen Y.B.,Wang Q.Q.,Wang X.,Jiang R.H.,Arredondo F.D.,Anderson R.G.,Thakur PB.,Mc Dowell J.M.,W ang Y.C.,and Tyler B.M.,2008Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b,The Plant Cell,20(4):1118-1133
Doyle E.A.,and Lambert K.N.,2003,Meloidogyne javanica chorismate mutase l alters plant cell development,Molecular Plant-Microbe Interactions,16(2):123-131
Flor H.H.,1971,Current status of the gene-for-gene concept Ann.Rev.Phytopathol.,9:275-296
Henderson I.R.,Navarro-Garcia F.,and Nataro J.P.,1998,The great escape:structure and function of the autotransporter proteins,Trends in Microbiol.,6(9):370-378
Hewezi T.,Howe P.,Maier T.R.,Hussey R.S.,Mitchum M.G.,Davis E.L.,and Baum T.J.,2008,Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase:cooperative cell wall modification during parasitism,The Plant Cell,20(11):3080-3093
Hewezi T.,Howe P.J.,Maier T.R.,Hussey R.S.,Mitchum M.G.,Davis E.L.,and Baum T.J.,2010,Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii,Plant Physiol.,152(2):968-984
Hewezi T.,Juvale P.S.,Piya S.,Maier T.R.,Rambani A.,Rice J.H.,Mitchum M.G.,Davis E.L.,Hussey R.S.,and Baum T.J.,2015,The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis,The Plant Cell,27(3):891-907
Hiss J.A.,Przyborski J.M.,Schwarte F.,Lingelbach K.,and Schneider G.,2008,The Plasmodium export element revisited,PLo S One,3(2):e1560
Hogenhout S.A.,Van der Hoorn R.A.,Terauchi R.,and Kamoun S.,2009,Emerging concepts in effector biology of plantassociated organisms,Molecular Plant-Microbe Interactions,22(2):115-122
Iberkleid I.,Vieira P.,de Almeida Engler J.,Firester K.,Spiegel Y.,and Horowitz S.B.,2013,Fatty acid-and retinol-binding protein,Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes,PLo S One,8(5):e64586
Jones J.D.,and Dangle J.L.,2006,The plant immune system,Nature,444(7117):323-329
Kvitko B.H.,Park D.H.,Velásquez A.C.,Wei C.F.,Russell A.B.,Martin G.B.,Schneider D.J.,and Collmer A.,2009,Deletions in the repertoire of Pseudomonas syringae pv.tomato DC300 0 typeⅢsecretion effector genes reveal functional overlap among effectors,PLo S Pathogens,5(4):e1000388
Lee C.,Chronis D.,Kenning C.,Peret B.,Hewezi T.,Davis E.L.,Baum T.J.,Hussey R.,Bennett M.,and Mitchum M.G.,2011,The novel cyst nematode effector protein 19C07interacts with the Arabidopsis auxin influx transporter LAX3to control feeding site development,Plant Physiol.,155(2):866-880
Lin B.R.,Zhuo K.,Wu P.,Cui R.Q.,Zhang L.H.,and Liao J.L.,2013,A novel effector pr otein,MJ-NULG1a,targeted to giant cell nuclei plays a role in Meloidogyne javanica parasitism,Molecular Plant-Microbe Interactions,26(1):55-66
Lindeberg M.,Stavrinides J.,Chang J.H.,Alfano J.R.,Collmer A.Dangl J.L.,Greenberg J.T.,Mansfield J.W.,and Guttman DS.,2005,Proposed guidelines for an unified nomenclature and phylogenetic analysis of typeⅢHop effector proteins in the plant pathogen Pseudomonas syringae,Mol.Plant Microbe Interact,18(4):275-282
Liu Y.,2012,Preliminary study of candidate effector gene of Rhizoctonia solani and resistance gene of sheath blight Thesis for M.S.,Sichuan Agricultural University,Supervisor Zheng A.P.,pp.7-8(刘尧,2012,水稻纹枯病菌候选效应因子及抗纹枯病基因的初步研究,硕士学位论文,四川农业大学,导师:郑爱萍,pp.7-8)
Ma Z.C.,Zhu L.,Song T.Q.,Wang Y.,Zhang Q.,Xia Y.Q.,Qiu M.,Lin Y.C.,Li H.Y.,Kong L.,Fang Y.F.,Ye W.W.,Wang Y.,Dong S.M.,Zheng X.B.,Tyler B.M.,and Wang Y.C.2017,A paralogous decoy protects Phytophthora sojae apoplastic effector Ps XEG1 from a host inhibitor,Science355(6326):710-714
Mudgett M.B.,2005,New insights into the function of phytopathogenic bacterial typeⅢeffectors in plants,Annu Rev.Plant Biol.,56:509-531
Nunes M.C.,Goldring J.P.,Doerig C.,and Scherf A.,2007,Anovel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell,Molecular Microbiology,63(2):391-403
Rehmany A.P.,Gordon A.,Rose L.E.,Allen R.L.,Armstrong MR.,Whisson S.C.,Kamoun S.,Tyler B.M.,Birch P.R.,and Beynon J.L.,2005,Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1resistance genes from two Arabidopsis lines,Plant Cell,17(6):1839-1850
Rosso M.N.,Hussey R.S.,Davis E.L.,Smant G.,Baum T.J.Abad P.,and Mitchum M.G.,2012;Nematode effector proteins:targets and functions in plant parasitism,Effectors in Plant-microbe Interactions,11:327-354
Sharma S.,Sharma S.,Hirabuchi A.,Yoshida K.,Fujisaki K.,Ito A.,Uemura A.,Terauchi R.,Kamoun S.,Sohn K.H.,Jones J.D.,and Saitoh H.,2013,Deployment of the Burkholderia glumae typeⅢsecretion system as an efficient tool for translocating pathogen effectors to monocot cells,The Plant Journal,74(4):701-712
Van der Hoorn R.A.,and Kamoun S.,2008,From guard to decoy:a new model for perception of plant pathogen effectors,The Plant Cell,20(8):2009-2017
Van Esse H.P.,Van't Klooster J.W.,Bolton M.D.,Yadeta K.A.,Van Baarlen P.,Boeren S.,Vervoort J.,de Wit P.J.,and Thomma B.P.,2008,The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense,The Plant Cell,20(7):1948-1963
Vivian A.,and Arnold D.L.,2000,Bacterial effector genes and their role in host-pathogen interactions,Journal of Plant Pathology,82(3):163-178
Wastie R.L.,ed.,1991,Breeding for resistance,In advances in plant pathology vol 7:Phytovhthora infestans,the cause of late blight of potato,Academic Press,London,pp.193-223
Whisson S.C.,Boevink P.C.,Moleleki L.,Avrova A.O.,Morales J.G.,Gilroy E.M.,Armstrong M.R.,Grouffaud S.,van West P.,Chapman S.,Hein I.,Toth I.K.,Pritchard L.,and Birch P.R.,2007,A translocation signal for delivery of oomycete effector proteins inside host plant cells,Nature,450(7166):115-118
Win J.,Morgan W.,Bos J.,Krasileva K.V.,Cano L.M.,Chaparro-Garcia A.,Ammar R.,Staskawicz B.J.,and Kamoun S.,2007,Adaptive evolution has targeted the C-terminal domain of the Rx LR effectors of plant pathogenic oomycetes,Plant Cell,19(8):2349-2369
Woo M.O.,Beard H.,Mac Donald M.H.,Brewer E.P.,Youssef R.M.,Kim H.,and Matthews B.F.,2014,Manipulation of twoα-endo-β-1,4-g lucanase genes,At Cel6 and Gm Cel7,reduces susceptibility to Heterodera glycines in soybean roots,Mol.Plant Pathol.,15(9):927-939
Xue B.Y.,Hamamouch N.,Li C.Y.,Huang G.,Hussey R.S.,Baum T.J.,and Davis E.L.,2013,The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots,Phytopathology,103(2):175-181
Anderson J.P.,Gleason C.A.,Foley R.C.,Thrall P.H.,Burdon JB.,and Singh K.B.,2010,Plants versus pathogens:an evolutionary arms race,Functional Plant Biology,37(6)499-512
Chen J.S.,Lin B.R.,Huang Q.L.,Hu L.L.,Zhuo K.,and Liao J.L.2017,A novel Meloidogyne graminicola effector,Mg GPP,is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism,PLo S Pathogens,13(4):e1006301
Chen Q.G.,Shu C.W.,Yang M.,and Zhou E.X.,2016,Research advance on the effectors of plant pathogenic fungi,Jiyinzuxue Yu Yingyong Shengwuxue(Genomics and Applied Biology)35(11):3105-3114(陈琦光,舒灿伟,杨媚,周而勋,2016植物病原真菌效应分子的研究进展,基因组学与应用生物学,35(11):3105-3114)
Chen Q.G.,Wangchen J.Z.,Yang M.,and Zhou E.X.,2015Prediction of candidate effectors from the genome of Colletotrichum higginsianum,Redai Zuowu Xuebao(Chinese Journal of Tropical Crops),36(6):1105-1111(陈琦光,王陈骄子,杨媚,周而勋,2015,希金斯刺盘孢全基因组候选效应分子的预测,热带作物学报,36(6):1105-1111)
Dangl J.L.,and Jones J.D.,2001,Plant pathogens and integrated defence responses to infection,Nature,411(6839):826-833
Davis E.L.,Hussey R.S.,Baum T.J.,Bakker J.,Schots A.,Rosso M.N.,and Abad P.,2000,Nematode:parasitism genes Annu.Rev.Phytopathol.,38(4):365-396
Davis E.L.,Hussey R.S.,Mitchum M.G.,and Baum T.J.,2008Parasitism proteins in nematode-plant interactions,Curr Opin.Plant Biol.,11(4):360-366
De Jonge R.,Van Esse H.P.,Kombrink A.,Shinya T.,Desaki Y.Bours R.,Van der Krol S.,Shibuya N.,Joosten M.H.,and Thomma B.P.,2010,Conserved fungal Lys M effector Ecp6prevents chitin-triggered immunity in plants,Science,329(5994):953-955
Dou D.L.,Kale S.D.,Wang X.L.,Chen Y.B.,Wang Q.Q.,Wang X.,Jiang R.H.,Arredondo F.D.,Anderson R.G.,Thakur PB.,Mc Dowell J.M.,W ang Y.C.,and Tyler B.M.,2008Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b,The Plant Cell,20(4):1118-1133
Doyle E.A.,and Lambert K.N.,2003,Meloidogyne javanica chorismate mutase l alters plant cell development,Molecular Plant-Microbe Interactions,16(2):123-131
Flor H.H.,1971,Current status of the gene-for-gene concept Ann.Rev.Phytopathol.,9:275-296
Henderson I.R.,Navarro-Garcia F.,and Nataro J.P.,1998,The great escape:structure and function of the autotransporter proteins,Trends in Microbiol.,6(9):370-378
Hewezi T.,Howe P.,Maier T.R.,Hussey R.S.,Mitchum M.G.,Davis E.L.,and Baum T.J.,2008,Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase:cooperative cell wall modification during parasitism,The Plant Cell,20(11):3080-3093
Hewezi T.,Howe P.J.,Maier T.R.,Hussey R.S.,Mitchum M.G.,Davis E.L.,and Baum T.J.,2010,Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii,Plant Physiol.,152(2):968-984
Hewezi T.,Juvale P.S.,Piya S.,Maier T.R.,Rambani A.,Rice J.H.,Mitchum M.G.,Davis E.L.,Hussey R.S.,and Baum T.J.,2015,The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis,The Plant Cell,27(3):891-907
Hiss J.A.,Przyborski J.M.,Schwarte F.,Lingelbach K.,and Schneider G.,2008,The Plasmodium export element revisited,PLo S One,3(2):e1560
Hogenhout S.A.,Van der Hoorn R.A.,Terauchi R.,and Kamoun S.,2009,Emerging concepts in effector biology of plantassociated organisms,Molecular Plant-Microbe Interactions,22(2):115-122
Iberkleid I.,Vieira P.,de Almeida Engler J.,Firester K.,Spiegel Y.,and Horowitz S.B.,2013,Fatty acid-and retinol-binding protein,Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes,PLo S One,8(5):e64586
Jones J.D.,and Dangle J.L.,2006,The plant immune system,Nature,444(7117):323-329
Kvitko B.H.,Park D.H.,Velásquez A.C.,Wei C.F.,Russell A.B.,Martin G.B.,Schneider D.J.,and Collmer A.,2009,Deletions in the repertoire of Pseudomonas syringae pv.tomato DC300 0 typeⅢsecretion effector genes reveal functional overlap among effectors,PLo S Pathogens,5(4):e1000388
Lee C.,Chronis D.,Kenning C.,Peret B.,Hewezi T.,Davis E.L.,Baum T.J.,Hussey R.,Bennett M.,and Mitchum M.G.,2011,The novel cyst nematode effector protein 19C07interacts with the Arabidopsis auxin influx transporter LAX3to control feeding site development,Plant Physiol.,155(2):866-880
Lin B.R.,Zhuo K.,Wu P.,Cui R.Q.,Zhang L.H.,and Liao J.L.,2013,A novel effector pr otein,MJ-NULG1a,targeted to giant cell nuclei plays a role in Meloidogyne javanica parasitism,Molecular Plant-Microbe Interactions,26(1):55-66
Lindeberg M.,Stavrinides J.,Chang J.H.,Alfano J.R.,Collmer A.Dangl J.L.,Greenberg J.T.,Mansfield J.W.,and Guttman DS.,2005,Proposed guidelines for an unified nomenclature and phylogenetic analysis of typeⅢHop effector proteins in the plant pathogen Pseudomonas syringae,Mol.Plant Microbe Interact,18(4):275-282
Liu Y.,2012,Preliminary study of candidate effector gene of Rhizoctonia solani and resistance gene of sheath blight Thesis for M.S.,Sichuan Agricultural University,Supervisor Zheng A.P.,pp.7-8(刘尧,2012,水稻纹枯病菌候选效应因子及抗纹枯病基因的初步研究,硕士学位论文,四川农业大学,导师:郑爱萍,pp.7-8)
Ma Z.C.,Zhu L.,Song T.Q.,Wang Y.,Zhang Q.,Xia Y.Q.,Qiu M.,Lin Y.C.,Li H.Y.,Kong L.,Fang Y.F.,Ye W.W.,Wang Y.,Dong S.M.,Zheng X.B.,Tyler B.M.,and Wang Y.C.2017,A paralogous decoy protects Phytophthora sojae apoplastic effector Ps XEG1 from a host inhibitor,Science355(6326):710-714
Mudgett M.B.,2005,New insights into the function of phytopathogenic bacterial typeⅢeffectors in plants,Annu Rev.Plant Biol.,56:509-531
Nunes M.C.,Goldring J.P.,Doerig C.,and Scherf A.,2007,Anovel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell,Molecular Microbiology,63(2):391-403
Rehmany A.P.,Gordon A.,Rose L.E.,Allen R.L.,Armstrong MR.,Whisson S.C.,Kamoun S.,Tyler B.M.,Birch P.R.,and Beynon J.L.,2005,Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1resistance genes from two Arabidopsis lines,Plant Cell,17(6):1839-1850
Rosso M.N.,Hussey R.S.,Davis E.L.,Smant G.,Baum T.J.Abad P.,and Mitchum M.G.,2012;Nematode effector proteins:targets and functions in plant parasitism,Effectors in Plant-microbe Interactions,11:327-354
Sharma S.,Sharma S.,Hirabuchi A.,Yoshida K.,Fujisaki K.,Ito A.,Uemura A.,Terauchi R.,Kamoun S.,Sohn K.H.,Jones J.D.,and Saitoh H.,2013,Deployment of the Burkholderia glumae typeⅢsecretion system as an efficient tool for translocating pathogen effectors to monocot cells,The Plant Journal,74(4):701-712
Van der Hoorn R.A.,and Kamoun S.,2008,From guard to decoy:a new model for perception of plant pathogen effectors,The Plant Cell,20(8):2009-2017
Van Esse H.P.,Van't Klooster J.W.,Bolton M.D.,Yadeta K.A.,Van Baarlen P.,Boeren S.,Vervoort J.,de Wit P.J.,and Thomma B.P.,2008,The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense,The Plant Cell,20(7):1948-1963
Vivian A.,and Arnold D.L.,2000,Bacterial effector genes and their role in host-pathogen interactions,Journal of Plant Pathology,82(3):163-178
Wastie R.L.,ed.,1991,Breeding for resistance,In advances in plant pathology vol 7:Phytovhthora infestans,the cause of late blight of potato,Academic Press,London,pp.193-223
Whisson S.C.,Boevink P.C.,Moleleki L.,Avrova A.O.,Morales J.G.,Gilroy E.M.,Armstrong M.R.,Grouffaud S.,van West P.,Chapman S.,Hein I.,Toth I.K.,Pritchard L.,and Birch P.R.,2007,A translocation signal for delivery of oomycete effector proteins inside host plant cells,Nature,450(7166):115-118
Win J.,Morgan W.,Bos J.,Krasileva K.V.,Cano L.M.,Chaparro-Garcia A.,Ammar R.,Staskawicz B.J.,and Kamoun S.,2007,Adaptive evolution has targeted the C-terminal domain of the Rx LR effectors of plant pathogenic oomycetes,Plant Cell,19(8):2349-2369
Woo M.O.,Beard H.,Mac Donald M.H.,Brewer E.P.,Youssef R.M.,Kim H.,and Matthews B.F.,2014,Manipulation of twoα-endo-β-1,4-g lucanase genes,At Cel6 and Gm Cel7,reduces susceptibility to Heterodera glycines in soybean roots,Mol.Plant Pathol.,15(9):927-939
Xue B.Y.,Hamamouch N.,Li C.Y.,Huang G.,Hussey R.S.,Baum T.J.,and Davis E.L.,2013,The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots,Phytopathology,103(2):175-181