丁香假单胞杆菌Avr基因与寄主植物R基因的互作研究进展
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摘要
细菌、卵菌以及真菌体内广泛存在着一类分泌蛋白即效应因子(effector),它们在病原微生物和寄主互作过程中发挥着重要作用。根据病原微生物与寄主是否属于亲和性互作,效应因子可分为毒性效应因子(Vir)和无毒效应因子(Avr)。介绍了模式病原细菌丁香假单胞杆菌的效应因子和寄主植物体内的R基因,阐述了Avr基因与R基因的互作机制,包括直接识别和间接识别。最后讨论与展望了丁香假单胞杆菌效应因子与植物R基因的互作研究在植物抗病育种上的重要参考价值。
Effectors, kind of secreted proteins, are widely existed in bacteria, oomycetes and fungi, which plays an important role in the interaction between pathogenic microorganisms and their hosts. Effectors are classified into avirulence effectors(Avr) and virulence effectors(Vir) according to whether pathogen can compatibly interact with its host or not. This paper introduced the efforts in the typical pathogenic bacteria Pseudomonas syringae and the R genes in host plants, and described the interaction mechanism between Avr genes and R genes, including direct recognition and indirect recognition. Moreover, we discussed and prospected the value of interaction research between Pseudomonas syringae effectors and plant R genes in plant disease resistance breeding.
Effectors, kind of secreted proteins, are widely existed in bacteria, oomycetes and fungi, which plays an important role in the interaction between pathogenic microorganisms and their hosts. Effectors are classified into avirulence effectors(Avr) and virulence effectors(Vir) according to whether pathogen can compatibly interact with its host or not. This paper introduced the efforts in the typical pathogenic bacteria Pseudomonas syringae and the R genes in host plants, and described the interaction mechanism between Avr genes and R genes, including direct recognition and indirect recognition. Moreover, we discussed and prospected the value of interaction research between Pseudomonas syringae effectors and plant R genes in plant disease resistance breeding.
引文
[1] Dangl J L, Jones J D. Plant pathogens and integrated defence responses to infection [J]. Nature, 2001, 411(6839):826-833.
[2] Haapalainen M, Dauphin A, Li C M, et al.. HrpZ harpins from different Pseudomonas syringae, pathovars differ in molecular interactions and in induction of anion channel responses in Arabidopsis thaliana, suspension cells[J]. Plant Physiol. Biochem., 2012, 51(2):168-174.
[3] Dillon M M, Thakur S, Almeida R N D, et al.. Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex[J]. Genome Biol., 2019, 20(1): 3.
[4] Hogenhout S A, Ra V D H, Terauchi R, et al.. Emerging concepts in effector biology of plant-associated organisms[J]. Mol. Plant Microb. Int., 2009, 22(2):115-122.
[5] 陈琦光, 舒灿伟, 杨媚, 等. 植物病原真菌效应分子的研究进展[J]. 基因组学与应用生物学, 2016(11):249-258.
[6] Mota L J, Cornelis G R. The bacterial injection kit: Type III secretion systems[J]. Ann. Med., 2005, 37(4):234-249.
[7] Alfano J R, Collmer A. The type III (Hrp) secretion pathway of plant pathogenic bacteria: Trafficking harpins, Avr proteins, and death[J]. J. Bacteriol., 1997, 179(18):5655-5662.
[8] Henderson, Ian R, Navarro G, et al.. The great escape: Structure and function of the autotransporter proteins[J]. Trends Microbiol., 1998, 6(9):370-378.
[9] Koebnik R. The role of bacterial pili in protein and DNA translocation[J]. Trends Microbiol., 2001, 9(12):586-590.
[10] Grant S R, Fisher E J, Chang J H, et al.. Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria[J]. Ann. Rev. Microbiol., 2006, 60(60):425-449.
[11] Mudgett M B. New insights to the function of phytopathogenic bacterial type III effectors in plants [J]. Ann. Rev. Plant Biol., 2005, 56(1):509-531.
[12] 李金玥. 植物病原菌效应因子的毒性功能研究进展[J]. 科教导刊, 2016(12):25-27.
[13] Noel L, Thieme F, Nennstiel D, et al.. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island[J]. J. Bacteriol., 2002, 184(5):1340-1348.
[14] He S Y, Huang H C, Collmer A. Pseudomonas syringae pv. syringae harpin Pss: A protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants [J]. Cell, 1993, 73(7):1255-1266.
[15] Lindgren P B. The role of hrp genes during plant-bacterial interactions [J]. Ann. Rev. Phytopathol., 1997, 35(1):129-152.
[16] Jin Q, Thilmony R, Zwieslervollick J, et al.. Type III protein secretion in Pseudomonas syringae[J]. Science, 2001, 294(5551):2556-2558.
[17] Li C M, Brown I, Mansfield J, et al.. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ[J]. Embo. J., 2014, 21(8):1909-1915.
[18] Alfano J R, Collmer A. Type III secretion system effector proteins: Double agents in bacterial disease and plant defense [J]. Ann. Rev. Phytopathol., 2004, 42(42):385-414.
[19] Büttner D. Getting across—bacterial type III effector proteins on their way to the plant cell[J]. Embo. J., 2014, 21(20):5313-5322.
[20] Mudgett M B. New insights to the function of phytopathogenic bacterial type III effectors in plants [J]. Ann. Rev. Plant Biol., 2005, 56(1):509-531.
[21] Block A, Li G, Fu Z Q, et al.. Phytopathogen type III effector weaponry and their plant targets[J]. Curr. Opin. Plant Biol., 2008, 11(4):396-403.
[22] Block A, Alfano J R. Plant targets for Pseudomonas syringae type III effectors: Virulence targets or guarded decoys?[J]. Curr. Opin. Microbiol., 2011, 14(1):39-46.
[23] Jackson R W, Athanassopoulos E, Tsiamis G, et al.. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola [J]. Proc. Natl. Acad. Sci. USA, 1999, 96(19):10875-10880.
[24] Wang Y, Li J, Hou S, et al.. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinases [J]. Plant Cell, 2010, 22(6):2033-2044.
[25] Zhang J, Shao F, Li Y, et al.. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants[J]. Cell Host Microb., 2007, 1(3): 175-185.
[26] Wilton M, Dangl J L. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence[J]. Proc. Natl. Acad. Sci. USA, 2010, 107(6):2349-2354.
[27] Anna B, Tania Y, Elowsky C G, et al.. The Pseudomonas syringae, type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9[J]. New Phytol., 2014, 201(4):1358-1370.
[28] 王国勋, 李磊, 周俭民. 病原效应蛋白HopB1抑制植物的天然免疫反应[J]. 遗传, 2016, 38(12):1110-1111.
[29] Shimono M, Lu Y J, Porter K, et al.. The Pseudomonas syringae type-III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection[J]. Plant Physiol., 2016, 171(3):2239-2255.
[30] Washington E J, Mukhtar M S, Finkel O M, et al.. Pseudomonas syringae type III effector HopAF1 suppresses plant immunity by targeting methionine recycling to block ethylene induction[J]. Proc. Natl. Acad. Sci. USA, 2016, 113(25): E3577-E3586.
[31] Li Y, Teixeira P J P L, Biswas S, et al.. Pseudomonas syringae, type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence[J]. Cell Host Microb., 2017, 21(2):156–168.
[32] Staskawicz B J, Dahlbeck D, Keen N T. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr[J]. Proc. Natl. Acad. Sci. USA, 1984, 81(19):6024-6028.
[33] Napoli C, Staskawicz B. Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea[J]. J. Bacteriol., 1987, 169(2):572-578.
[34] Axtell M J, Staskawicz B J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4[J]. Cell, 2003, 112(3):369-377.
[35] Mackey D, Belkhadir Y, Alonso J M, et al.. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance[J]. Cell, 2003, 112(3):379-389.
[36] 崔福浩.丁香假单胞效应蛋白AvrRpt2抑制植物免疫分子机制的研究[D]. 北京:中国农业大学,硕士学位论文, 2013.
[37] Mackey D, Iii B F H, Wiig A, et al.. RIN4 Interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis[J]. Cell, 2002, 108(6):750-754.
[38] 李魏. 拟南芥U-box蛋白PUB13的功能研究[D]. 长沙:湖南农业大学,博士学位论文, 2012.
[39] Abramovitch R B, Martin G B. AvrPtoB: A bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity[J]. FEMS Biotechnol. Lett. Ban.,2005, 245(1):1-8.
[40] 张月娟, 朱秀秀, 陈新, 等. 番茄细菌性斑点病菌无毒基因研究进展[J]. 植物保护, 2008, 34(4):12-18.
[41] Geng X, Shen M, Kim J H, et al.. The Pseudomonas syringae type III effectors AvrRpm1 and AvrRpt2 promote virulence dependent on the F-box protein COI1[J]. Plant Cell Rep., 2016, 35(4):921-932.
[42] Flor H H. Current status of the gene-for-gene concept[J]. Ann. Rev. Phytopathol., 1971, 9(1):275-296.
[43] Tang X, Frederick R D, Zhou J, et al.. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase[J]. Science, 1996, 274(5295):2060-2063.
[44] Van E D B, Jones J D. Plant disease-resistance proteins and the gene-for-gene concept[J]. Trends Biochem. Sci., 1998, 23(12):454-456.
[45] Shao F, Golstein C, Ade J, et al.. Cleavage of Arabidopsis PBS1 by a bacterial type III effector[J]. Science, 2003, 301(5637):1230-1233.
[46] Tasset C, Bernoux M, Jauneau A, et al.. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis[J]. PLoS Pathog., 2010, 6(11):e1001202.
[47] Chisholm S T, Dahlbeck D, Krishnamurthy N, et al.. Molecular characterization of proteolytic cleavage sites of the Pseudomonassyringae effector AvrRpt2 [J]. Proc. Natl Acad. Sci. USA, 2005, 102(6): 2087-2092.
[48] Van R D H, Kamoun S. From guard to decoy: A new model for perception of plant pathogen effectors[J]. Plant Cell, 2008, 20(8):2009-2017.
[49] Zhang J, Li W, Xiang T, et al.. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector[J]. Cell Host Microb., 2010, 7(4): 290-301.
[50] Dodds P N, Rathjen J P. Plant immunity: Towards an integrated view of plant-pathogen interactions[J]. Nat. Rev. Genet., 2010, 11(8):539-548.
[51] Zhan J, Thrall P H, Papa?x J, et al.. Playing on a pathogen's weakness: Using evolution to guide sustainable plant disease control strategies [J]. Ann. Rev. Phytopathol., 2015, 53(1):19-43.
[2] Haapalainen M, Dauphin A, Li C M, et al.. HrpZ harpins from different Pseudomonas syringae, pathovars differ in molecular interactions and in induction of anion channel responses in Arabidopsis thaliana, suspension cells[J]. Plant Physiol. Biochem., 2012, 51(2):168-174.
[3] Dillon M M, Thakur S, Almeida R N D, et al.. Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex[J]. Genome Biol., 2019, 20(1): 3.
[4] Hogenhout S A, Ra V D H, Terauchi R, et al.. Emerging concepts in effector biology of plant-associated organisms[J]. Mol. Plant Microb. Int., 2009, 22(2):115-122.
[5] 陈琦光, 舒灿伟, 杨媚, 等. 植物病原真菌效应分子的研究进展[J]. 基因组学与应用生物学, 2016(11):249-258.
[6] Mota L J, Cornelis G R. The bacterial injection kit: Type III secretion systems[J]. Ann. Med., 2005, 37(4):234-249.
[7] Alfano J R, Collmer A. The type III (Hrp) secretion pathway of plant pathogenic bacteria: Trafficking harpins, Avr proteins, and death[J]. J. Bacteriol., 1997, 179(18):5655-5662.
[8] Henderson, Ian R, Navarro G, et al.. The great escape: Structure and function of the autotransporter proteins[J]. Trends Microbiol., 1998, 6(9):370-378.
[9] Koebnik R. The role of bacterial pili in protein and DNA translocation[J]. Trends Microbiol., 2001, 9(12):586-590.
[10] Grant S R, Fisher E J, Chang J H, et al.. Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria[J]. Ann. Rev. Microbiol., 2006, 60(60):425-449.
[11] Mudgett M B. New insights to the function of phytopathogenic bacterial type III effectors in plants [J]. Ann. Rev. Plant Biol., 2005, 56(1):509-531.
[12] 李金玥. 植物病原菌效应因子的毒性功能研究进展[J]. 科教导刊, 2016(12):25-27.
[13] Noel L, Thieme F, Nennstiel D, et al.. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island[J]. J. Bacteriol., 2002, 184(5):1340-1348.
[14] He S Y, Huang H C, Collmer A. Pseudomonas syringae pv. syringae harpin Pss: A protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants [J]. Cell, 1993, 73(7):1255-1266.
[15] Lindgren P B. The role of hrp genes during plant-bacterial interactions [J]. Ann. Rev. Phytopathol., 1997, 35(1):129-152.
[16] Jin Q, Thilmony R, Zwieslervollick J, et al.. Type III protein secretion in Pseudomonas syringae[J]. Science, 2001, 294(5551):2556-2558.
[17] Li C M, Brown I, Mansfield J, et al.. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ[J]. Embo. J., 2014, 21(8):1909-1915.
[18] Alfano J R, Collmer A. Type III secretion system effector proteins: Double agents in bacterial disease and plant defense [J]. Ann. Rev. Phytopathol., 2004, 42(42):385-414.
[19] Büttner D. Getting across—bacterial type III effector proteins on their way to the plant cell[J]. Embo. J., 2014, 21(20):5313-5322.
[20] Mudgett M B. New insights to the function of phytopathogenic bacterial type III effectors in plants [J]. Ann. Rev. Plant Biol., 2005, 56(1):509-531.
[21] Block A, Li G, Fu Z Q, et al.. Phytopathogen type III effector weaponry and their plant targets[J]. Curr. Opin. Plant Biol., 2008, 11(4):396-403.
[22] Block A, Alfano J R. Plant targets for Pseudomonas syringae type III effectors: Virulence targets or guarded decoys?[J]. Curr. Opin. Microbiol., 2011, 14(1):39-46.
[23] Jackson R W, Athanassopoulos E, Tsiamis G, et al.. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola [J]. Proc. Natl. Acad. Sci. USA, 1999, 96(19):10875-10880.
[24] Wang Y, Li J, Hou S, et al.. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinases [J]. Plant Cell, 2010, 22(6):2033-2044.
[25] Zhang J, Shao F, Li Y, et al.. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants[J]. Cell Host Microb., 2007, 1(3): 175-185.
[26] Wilton M, Dangl J L. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence[J]. Proc. Natl. Acad. Sci. USA, 2010, 107(6):2349-2354.
[27] Anna B, Tania Y, Elowsky C G, et al.. The Pseudomonas syringae, type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9[J]. New Phytol., 2014, 201(4):1358-1370.
[28] 王国勋, 李磊, 周俭民. 病原效应蛋白HopB1抑制植物的天然免疫反应[J]. 遗传, 2016, 38(12):1110-1111.
[29] Shimono M, Lu Y J, Porter K, et al.. The Pseudomonas syringae type-III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection[J]. Plant Physiol., 2016, 171(3):2239-2255.
[30] Washington E J, Mukhtar M S, Finkel O M, et al.. Pseudomonas syringae type III effector HopAF1 suppresses plant immunity by targeting methionine recycling to block ethylene induction[J]. Proc. Natl. Acad. Sci. USA, 2016, 113(25): E3577-E3586.
[31] Li Y, Teixeira P J P L, Biswas S, et al.. Pseudomonas syringae, type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence[J]. Cell Host Microb., 2017, 21(2):156–168.
[32] Staskawicz B J, Dahlbeck D, Keen N T. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr[J]. Proc. Natl. Acad. Sci. USA, 1984, 81(19):6024-6028.
[33] Napoli C, Staskawicz B. Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea[J]. J. Bacteriol., 1987, 169(2):572-578.
[34] Axtell M J, Staskawicz B J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4[J]. Cell, 2003, 112(3):369-377.
[35] Mackey D, Belkhadir Y, Alonso J M, et al.. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance[J]. Cell, 2003, 112(3):379-389.
[36] 崔福浩.丁香假单胞效应蛋白AvrRpt2抑制植物免疫分子机制的研究[D]. 北京:中国农业大学,硕士学位论文, 2013.
[37] Mackey D, Iii B F H, Wiig A, et al.. RIN4 Interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis[J]. Cell, 2002, 108(6):750-754.
[38] 李魏. 拟南芥U-box蛋白PUB13的功能研究[D]. 长沙:湖南农业大学,博士学位论文, 2012.
[39] Abramovitch R B, Martin G B. AvrPtoB: A bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity[J]. FEMS Biotechnol. Lett. Ban.,2005, 245(1):1-8.
[40] 张月娟, 朱秀秀, 陈新, 等. 番茄细菌性斑点病菌无毒基因研究进展[J]. 植物保护, 2008, 34(4):12-18.
[41] Geng X, Shen M, Kim J H, et al.. The Pseudomonas syringae type III effectors AvrRpm1 and AvrRpt2 promote virulence dependent on the F-box protein COI1[J]. Plant Cell Rep., 2016, 35(4):921-932.
[42] Flor H H. Current status of the gene-for-gene concept[J]. Ann. Rev. Phytopathol., 1971, 9(1):275-296.
[43] Tang X, Frederick R D, Zhou J, et al.. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase[J]. Science, 1996, 274(5295):2060-2063.
[44] Van E D B, Jones J D. Plant disease-resistance proteins and the gene-for-gene concept[J]. Trends Biochem. Sci., 1998, 23(12):454-456.
[45] Shao F, Golstein C, Ade J, et al.. Cleavage of Arabidopsis PBS1 by a bacterial type III effector[J]. Science, 2003, 301(5637):1230-1233.
[46] Tasset C, Bernoux M, Jauneau A, et al.. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis[J]. PLoS Pathog., 2010, 6(11):e1001202.
[47] Chisholm S T, Dahlbeck D, Krishnamurthy N, et al.. Molecular characterization of proteolytic cleavage sites of the Pseudomonassyringae effector AvrRpt2 [J]. Proc. Natl Acad. Sci. USA, 2005, 102(6): 2087-2092.
[48] Van R D H, Kamoun S. From guard to decoy: A new model for perception of plant pathogen effectors[J]. Plant Cell, 2008, 20(8):2009-2017.
[49] Zhang J, Li W, Xiang T, et al.. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector[J]. Cell Host Microb., 2010, 7(4): 290-301.
[50] Dodds P N, Rathjen J P. Plant immunity: Towards an integrated view of plant-pathogen interactions[J]. Nat. Rev. Genet., 2010, 11(8):539-548.
[51] Zhan J, Thrall P H, Papa?x J, et al.. Playing on a pathogen's weakness: Using evolution to guide sustainable plant disease control strategies [J]. Ann. Rev. Phytopathol., 2015, 53(1):19-43.