The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death

New Phytologist

Volumn 196, Issue 1, 2012, Pages 247-260

  Yu, Xiaoli ^a   Tang, Junli ^a   Wang, Qunqing ^a   Ye, Wenwu ^a   Tao, Kai ^a   Duan, Shuyi ^a   Lu, Chenchen ^a   Yang, Xinyu ^a   Dong, Suomeng ^a   Zheng, Xiaobo ^a   Wang, Yuanchao ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cell death; Localization; Phytophthora sojae; Plasma membrane; RxLR effector; Virulence

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN;

CELL ORGANELLE; GENOME; IMMUNE SYSTEM; INFECTIVITY; MEMBRANE; MOLECULAR ANALYSIS; PATHOGEN; PLANT DEFENSE; PROTEIN; SOYBEAN; TOBACCO; VIRULENCE;

AMINO ACID SEQUENCE; ARTICLE; CELL DEATH; CELL FRACTIONATION; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENE DELETION; GENE SILENCING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYTOPHTHORA; PLANT CELL; PLANT DISEASE; PLANT IMMUNITY; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SPECIES DIFFERENCE; TOBACCO; VIRULENCE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL DEATH; CELL MEMBRANE; GENE DELETION; GENE SILENCING; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; PHYTOPHTHORA; PLANT CELLS; PLANT DISEASES; PLANT IMMUNITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEINS; SPECIES SPECIFICITY; SUBCELLULAR FRACTIONS; TOBACCO; VIRULENCE;

GLYCINE MAX; NICOTIANA BENTHAMIANA; PHYTOPHTHORA; PHYTOPHTHORA CAPSICI; PHYTOPHTHORA SOJAE;

EID: 84865553765     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04241.x     Document Type: Article

References (81)

1. Armstrong MR, Whisson SC, Pritchard L, Bos JI, Venter E, Avrova AO, Rehmany AP, Bohme U, Brooks K, Cherevach I et al. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences, USA 102: 7766-7771.
2. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
3. Baulcombe DC. 1999. Fast forward genetics based on virus-induced gene silencing. Current Opinion in Plant Biology 2: 109-113.
4. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
5. Birch PR, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC. 2008. Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Current Opinion in Plant Biology 11: 373-379.
6. Bos JI, Kanneganti TD, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PR, Kamoun S. 2006. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant Journal 48: 165-176.
7. Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Zhendong T, Engelhardt S, Vetukuri RR, Harrower B et al. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences, USA 107: 9909-9914.
8. Boutemy LS, King SR, Win J, Hughes RK, Clarke TA, Blumenschein TM, Kamoun S, Banfield MJ. 2011. Structures of Phytophthora RXLR effector proteins: a conserved but adaptable fold underpins functional diversity. Journal of Biological Chemistry 286: 35834-35842.
9. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, Cano LM, Jones AM, Huitema E, van der Hoorn RA et al. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proceedings of the National Academy of Sciences, USA 108: 20832-20837.
10. Caillaud MC, Piquerez SJ, Fabro G, Steinbrenner J, Ishaque N, Beynon J, Jones JD. 2012. Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant Journal 69: 252-265.
11. Chen S, Songkumarn P, Liu J, Wang GL. 2009. A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiology 150: 1111-1121.
12. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
13. Dangl JL, Jones JD. 2001. Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
14. De Wit PJ, Mehrabi R, Van den Burg HA, Stergiopoulos I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10: 735-747.
15. Dong S, Mackey D, Yin W, Kong G, Yang X, Qutob D, Chen Q, Kale SD, Sui Y, Zhang Z et al. 2011b. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. PLoS Pathogens 7: e1002353.
16. Dong S, Qutob D, Tedman-Jones J, Kuflu K, Wang Y, Tyler BM, Gijzen M. 2009. The Phytophthora sojae avirulence locus Avr3c encodes a multi-copy RXLR effector with sequence polymorphisms among pathogen strains. PLoS ONE 4: e5556.
17. Dong S, Yu D, Cui L, Qutob D, Tedman-Jones J, Kale SD, Tyler BM, Wang Y, Gijzen M. 2011a. Sequence variants of the Phytophthora sojae RXLR effector Avr3a/5 are differentially recognized by Rps3a and Rps5 in soybean. PLoS ONE 6: e20172.
18. Dong S, Zhang Z, Zheng X, Wang Y. 2008. Mammalian pro-apoptotic bax gene enhances tobacco resistance to pathogens. Plant Cell Reports 27: 1559-1569.
19. Dou D, Kale SD, Liu T, Tang Q, Wang X, Arredondo FD, Basnayake S, Whisson S, Drenth A, Maclean D et al. 2010. Different domains of Phytophthora sojae effector Avr4/6 are recognized by soybean resistance genes Rps4 and Rps6. Molecular Plant-Microbe Interactions 23: 425-435.
20. Dou D, Kale SD, Wang X, Chen Y, Wang Q, Jiang RH, Arredondo FD, Anderson RG, Thakur PB, McDowell JM et al. 2008a. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20: 1118-1133.
21. Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, Tyler BM. 2008b. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. The Plant Cell 20: 1930-1947.
22. Erwin DC, Ribeiro OK. 1996. Phytophthora diseases worldwide. St Paul, Minnesota, USA: The American Phytopathological Society, APS Press.
23. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5: 199-206.
24. Forster H, Tyler BM, Coffey MD. 1994. Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. MPMI-Molecular Plant Microbe Interactions 7: 780-791.
25. Gijzen M, Forster H, Coffey MD, Tyler B. 1996. Cosegregation of Avr4 and Avr6 in Phytophthora sojae. Canadian Journal of Botany 74: 800-802.
26. Gilroy EM, Breen S, Whisson SC, Squires J, Hein I, Kaczmarek M, Turnbull D, Boevink PC, Lokossou A, Cano LM et al. 2011. Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. New Phytologist 191: 763-776.
27. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
28. He P, Chintamanani S, Chen Z, Zhu L, Kunkel BN, Alfano JR, Tang X, Zhou JM. 2004. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant Journal 37: 589-602.
29. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM. 2000. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Molecular Biology 42: 819-832.
30. Huet JC, Mansion M, Pernollet JC. 1993. Amino acid sequence of the alpha-elicitin secreted by Phytophthora cactorum. Phytochemistry 34: 1261-1264.
31. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT. 2007. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Current Biology 17: 499-508.
32. Jiang RHY, Tripathy S, Govers F, Tyler BM. 2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences, USA 105: 4874-4879.
33. Jones DA, Takemoto D. 2004. Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. Current Opinion in Immunology 16: 48-62.
34. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
35. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T et al. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284-295.
36. Kamoun S, Klucher KM, Coffey MD, Tyler BM. 1993. A gene encoding a host-specific elicitor protein of Phytophthora parasitica. Molecular Plant-Microbe Interactions 6: 573-581.
37. Kamoun S, van der Lee T, van den Berg-Velthuis G, de Groot KE, Govers F. 1998. Loss of production of the elicitor protein INF1 in the clonal lineage US-1 of Phytophthora infestans. Phytopathology 88: 1315-1323.
38. Keller H, Blein JP, Bonnet P, Ricci P. 1996. Physiological and molecular characteristics of Elicitin-induced systemic acquired resistance in tobacco. Plant Physiology 110: 365-376.
39. Kelley BS, Lee S-J, Damasceno CMB, Chakravarthy S, Kim B-D, Martin GB, Rose JKC. 2010. A secreted effector protein (SNE1) from Phytophthora infestans is a broadly acting suppressor of programmed cell death. Plant Journal 62: 357-366.
40. Liu T, Ye W, Ru Y, Yang X, Gu B, Tao K, Lu S, Dong S, Zheng X, Shan W et al. 2010. Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiology 155: 490-501.
41. Lu R, Malcuit I, Moffett P, Ruiz MT, Peart J, Wu AJ, 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 Journal 22: 5690-5699.
42. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics 26: 403-410.
43. Marois E, Van den Ackerveken G, Bonas U. 2002. The xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Molecular Plant-Microbe Interactions 15: 637-646.
44. Mathur J, Koncz C. 1998. Establishment and maintenance of cell suspension cultures. Methods In Molecular Biology-Clifton Then Totowa 82: 27-30.
45. May KJ, Whisson SC, Zwart RS, Searle IR, Irwin JA, Maclean DJ, Carroll BJ, Drenth A. 2002. Inheritance and mapping of 11 avirulence genes in Phytophthora sojae. Fungal Genetics and Biology 37: 1-12.
46. Medzhitov R, Janeway CA Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91: 295-298.
47. Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, Inze D, Ellis BE. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proceedings of the National Academy of Sciences, USA 96: 14165-14170.
48. Naoumkina MA, He X, Dixon RA. 2008. Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula. BMC Plant Biology 8: 132.
49. Nelson BK, Cai X, Nebenfuhr A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant Journal 51: 1126-1136.
50. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 10774-10779.
51. Nurnberger T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198: 249-266.
52. Oh CS, Martin GB. 2010. Effector-triggered immunity mediated by the Pto kinase. Trends in Plant Science 16: 132-140.
53. Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, Cano LM, Win J, Bos JI, Liu HY, van Damme M et al. 2009. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928-2947.
54. Pedley KF, Martin GB. 2005. Role of mitogen-activated protein kinases in plant immunity. Current Opinion in Plant Biology 8: 541-547.
55. van Poppel PM, Guo J, van de Vondervoort PJ, Jung MW, Birch PR, Whisson SC, Govers F. 2008. The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Molecular Plant-Microbe Interactions 21: 1460-1470.
56. del Pozo O, Pedley KF, Martin GB. 2004. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO Journal 23: 3072-3082.
57. Qutob D, Tedman-Jones J, Dong S, Kuflu K, Pham H, Wang Y, Dou D, Kale SD, Arredondo FD, Tyler BM et al. 2009. Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS ONE 4: e5066.
58. Rabin SDP, Veesenmeyer JL, Bieging KT, Hauser AR. 2006. A C-terminal domain targets the Pseudomonas aeruginosa cytotoxin ExoU to the plasma membrane of host cells. Infection and Immunity 74: 2552-2561.
59. Robert-Seilaniantz A, Shan L, Zhou JM, Tang X. 2006. The Pseudomonas syringae pv. tomato DC3000 type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Molecular Plant-Microbe Interactions 19: 130-138.
60. Ruiz MT, Voinnet O, Baulcombe DC. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10: 937-946.
61. Schechter LM, Vencato M, Jordan KL, Schneider SE, Schneider DJ, Collmer A. 2006. Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Molecular Plant-Microbe Interactions 19: 1180-1192.
62. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Gaulin E, Kamoun S, Huitema E. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proceedings of the National Academy of Sciences, USA 107: 17421-17426.
63. Scott A, Wyatt S, Tsou PL, Robertson D, Allen NS. 1999. Model system for plant cell biology: GFP imaging in living onion epidermal cells. BioTechniques 26: 1125, 1128-1132.
64. Shan L, Thara VK, Martin GB, Zhou JM, Tang X. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12: 2323-2338.
65. Shan W, Cao M, Leung D, Tyler BM. 2004. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions 17: 394-403.
66. Stergiopoulos I, de Wit PJ. 2009. Fungal effector proteins. Annual review of Phytopathology 47: 233-263.
67. Takahashi Y, Nasir KHB, Ito A, Kanzaki H, Matsumura H, Saitoh H, Fujisawa S, Kamoun S, Terauchi R. 2007. A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant Journal 49: 1030-1040.
68. Thines M, Kamoun S. 2010. Oomycete-plant coevolution: recent advances and future prospects. Current Opinion in Plant Biology 13: 427-433.
69. Tyler BM. 2009. Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cellular Microbiology 11: 13-20.
70. Tyler BM, Forster H, Coffey MD. 1995. Inheritance of avirulence factors and restriction fragment length polymorphism markers in outcrosses of the oomycete Phytophthora sojae. Molecular Plant-Microbe Interactions 8: 515-523.
71. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.
72. Veesenmeyer JL, Howell H, Halavaty AS, Ahrens S, Anderson WF, Hauser AR. 2010. Role of the membrane localization domain of the Pseudomonas aeruginosa effector protein ExoU in cytotoxicity. Infection and Immunity 78: 3346-3357.
73. Vleeshouwers VG, Rietman H, Krenek P, Champouret N, Young C, Oh SK, Wang M, Bouwmeester K, Vosman B, Visser RG et al. 2008. Effector genomics accelerates discovery and functional profiling of potato disease resistance and phytophthora infestans avirulence genes. PLoS ONE 3: e2875.
74. Wang L, Tang X, He C. 2007. The bifunctional effector AvrXccC of Xanthomonas campestris pv. campestris requires plasma membrane-anchoring for host recognition. Molecular Plant Pathology 8: 491-501.
75. Wang Q, Han C, Ferreira AO, Yu X, Ye W, Tripathy S, Kale SD, Gu B, Sheng Y, Sui Y et al. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. The Plant Cell 23: 2064-2086.
76. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115-118.
77. Whisson SC, Drenth A, Maclean DJ, Irwin JA. 1994. Evidence for outcrossing in Phytophthora sojae and linkage of a DNA marker to two avirulence genes. Current Genetics 27: 77-82.
78. Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ. 2012. Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathogens 8: e1002400.
79. Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, Ammar R, Staskawicz BJ, Kamoun S. 2007. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19: 2349-2369.
80. Wu S, Lu D, Kabbage M, Wei HL, Swingle B, Records AR, Dickman M, He P, Shan L. 2011. Bacterial effector HopF2 suppresses Arabidopsis innate immunity at the plasma membrane. Molecular Plant-Microbe Interactions 24: 585-593.
81. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Current Biology 18: 74-80.