Hyaloperonospora arabidopsidis as a pathogen model

Annual Review of Phytopathology

Volumn 48, Issue , 2010, Pages 329-345

  Coates, Mary E ^a   Beynon, Jim L ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Arabidopsis thaliana; avirulence; coevolution; effector; oomycete

Indexed keywords

ARABIDOPSIS; ARTICLE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; OOMYCETES; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE;

ARABIDOPSIS; HOST-PATHOGEN INTERACTIONS; OOMYCETES; PLANT DISEASES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HYALOPERONOSPORA; OOMYCETES; PERONOSPORACEAE;

EID: 77956095798     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080508-094422     Document Type: Article

References (89)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95:10306-10311
2. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, et al. 2004. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957-1960
3. Allen RL, Meitz JC, Baumber RE, Hall SA, Lee SC, et al. 2008. Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol. Plant Pathol. 9:511-523
4. Angot A, Vergunst A, Genin S, Peeters N. 2007. Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3(1):e3
5. Armstrong MR, Whisson SC, Pritchard L, Bos JIB, Venter E, et al. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. USA 102:7766-7771
6. Bakker EG, Toomajian C, Kreitman M, Bergelson J. 2006. A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18:1803-1818
7. Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, et al. 2006. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2(5):e50
8. Birch PRJ, Armstrong M, Bos J, BoevinkP, Gilroy EM, et al. 2009. Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J. Exp. Bot. 60:1133-1140
9. Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC. 2008. Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11:373-379
10. Bittner-Eddy P, Can C, Gunn N, Pinel M, Tor M, et al. 1999. Genetic and physical mapping of the RPP13 locus, in Arabidopsis, responsible for specific recognition of several Peronospora parasitica (downy mildew) isolates. Mol. Plant-Microbe Interact. 12:792-802
11. Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL. 2000. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 21:177-188
12. Block A, Li GY, Fu ZQ, Alfano J.R. 2008. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11:396-403
13. Bos JIB, Kanneganti TD, Young C, Cakir C, Huitema E, et al. 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 J. 48:165-176
14. BotellaMA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, et al. 1998. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847-1860
15. Catanzariti AM, Dodds PN, EllisJG. 2007. Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol. Lett. 269:181-188
16. Century KS, Holub EB, Staskawicz BJ. 1995. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and fungal pathogen. Proc. Natl. Acad. Sci. USA 92:6597-6601
17. Chang HH, Falick AM, Carlton PM, SedatJW, Derisi JL, Marletta M.A. 2008. N-terminal processing of proteins exported by malaria parasites. Mol. Biochem. Parasitol. 160:107-115
18. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814
19. Constantinescu O, Fatehi J. 2002. Peronospora-like fungi (Chromista, Peronosporales) parasitic on Bras-sicaceae and related hosts. Nova Hedwigia 74:291-338
20. Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF. 2000. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663-676
21. Crute IR, Holub EB, Tor M, Brose E, Beynon JL. 1993. The identification and mapping of loci in Arabidopsis thaliana for recognition of the fungal pathogens Peronospora parasitica (downy mildew) and Albugo Candida (white blister). In Advances in the Molecular Genetics ofPlant-Microbe Interactions, ed. EW Nester, DPS Verma, 2:437-44. Dordrecht/Boston/London: Kluwer Acad. 617 pp.
22. Dangl JL, Holub EH, Debener T, Lehnackers H, Ritter C, Crute I. 1992. Genetic definition of loci involved in Arabidopisis-pathogen interactions. In Methods in Arabidopsis Research, ed. C Koncz, NH Chua, J Schell, 1:393-418. Singapore: World Sci. 496 pp.
23. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defense responses to infection. Nature 411:826-833
24. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ. 2009. A newly discovered protein export machine in malaria parasites. Nature 459:945-949
25. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, et al. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. USA 100:8024-8029
26. DingJ, Cheng HL,JinXQ,ArakiH, Yang YH,Tian DC. 2007. Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis. Genetica 129:235-242
27. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG. 2004. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16:755-768
28. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 103:8888-8893
29. Dong S, Qutob D, Tedman-Jones J, Kuflu K, Wang Y, et al. 2009. The Phytophthora sojae avirulence locus Avr3c encodes a multi-copy RXLR effector with sequence polymorphisms among pathogen strains. PLoS ONE 4:e5556
30. Dou DL, Kale SD, Wang XL, Chen YB, Wang QQ, et al. 2008. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20:1118-1133
31. Dou DL, Kale SD, Wang X, Jiang RHY, Bruce NA, et al. 2008. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20:1930-1947
32. Ellis JG, Dodds PN, Lawrence GJ. 2007. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu. Rev. Phytopathol. 45:289-306
33. Gaumann E. 1918. Ueber die formen der Peronospora parasitica (Pers.) Fries. Beih. Bot. Zentralblatt 35(1.Abt.):395-533
34. Goker M, Riethmiiller A, Voglmayr H, Weiss M, Oberwinkler F. 2004. Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycol. Prog. 3:83-94
35. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL. 2006. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60:425-449
36. Grouffaud S, van West P, Avrova AO, Birch PRJ, Whisson SC. 2008. Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154:3743-3751
37. Gunn ND, Byrne J, Holub EB. 2002. Outcrossing of two homothallic isolates of Peronospora parasitica and segregation of avirulence matching six resistance loci in Arabidopsis thaliana. In Advances in Downy Mildew Research, ed. PTN Spencer-Phillips, U Gisi, A Lebeda, 1:185-88. The Netherlands: Kluwer Acad. 267 pp.
38. Hall SA, Allen RL, Baumber RE, Baxter LA, Fisher K, et al. 2009. Maintenance of genetic variation in plants and pathogens involves complex networks of gene-for-gene interactions. Mol. Plant Pathol. 10:44957
39. Hardham AR. 2005. Phytophthora cinnamomi. Mol. Plant Pathol. 6:589-604
40. Hardham AR, Cahill DM, Cope M, Gabor BK, Gubler F, Hyde GJ. 1994. Cell surface antigens of Phytophthora spores: biological and taxonomic characterization. Protoplasma 181:213-232
41. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, et al. 2004. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934-1937
42. Holub E. 2006. Evolution of parasitic symbioses between plants and filamentous microorganisms. Curr. Opin. Plant Biol. 9:397-405
43. Holub EB. 2008. Natural history of Arabidopsis thaliana and oomycete symbioses. Eur. J. Plant Pathol. 122:91-109
44. Holub EB, Beynon JL. 1997. Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Adv. Bot. Res. 24:227-273
45. Holub EB, Beynon LJ, Crute IR. 1994. Phenotypic and genotypic characterization of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Mol. Plant-Microbe Interact. 7:223-239
46. Innes RW. 2004. Guarding the goods. New insights into the central alarm system of plants. Plant Physiol. 135:695-701
47. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19:4004-4014
48. 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. Proc. Natl. Acad. Sci. USA 105:4874-4879
49. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-329
50. Joos HJ, Mauch-Mani B, Slusarenko AJ. 1996. Molecular mapping of the Arabidopsis locus RPP11 which conditions isolate-specific hypersensitive resistance against downy mildew in ecotype RLD. Theor. Appl. Genet. 92:281-284
51. Kale SD, Gu B, Capelluto DGS, Dou D, Feldman E, et al. 2010. External phosphatidylinositol-3-phosphate mediates host cell entry by eukaryotic pathogen effectors. Cell In press
52. Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44:41-60
53. Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, et al. 2005. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol. Plant-Microbe Interact. 18:1130-1139
54. Koch E, Slusarenko A. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437-445
55. Latijnhouwers M, de Wit PJGM, Govers F. 2003. Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol. 11:462-469
56. Lindau G. 1901. Hilfsbuch fur das Sammein Parasitischer Pilze. Berlin: Borntrager Verlag
57. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, et al. 2008. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134:48-61
58. Marti M, Good RT, RugM, KnuepferE, Cowman AF. 2004. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930-1933
59. Mauch-Mani B, Slusarenko AJ. 1993. Arabidopsis as a model host for studying plant-pathogen interactions. Trends Microbiol. 1:265-270
60. Mauch-Mani B, Slusarenko AJ. 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203-212
61. McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S, et al. 1998. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of arabidopsis. Plant Cell 10:1861-1874
62. Mims CW, Richardson EA, Holt BFIII, Dangl JL. 2004. Ultrastructure of the host-pathogen interface in Arabidopsis thaliana leaves infected by the downy mildew Hyaloperonospora parasitica. Can. J. Bot., 82: 1001-1008
63. Morgan W, Kamoun S. 2007. RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol. 10:332-338
64. Noel L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, et al. 1999. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099-2111
65. Parker JE, Coleman MJ, Szabo V, Frost LN, Schmidt R, et al. 1997. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the Toll and Interleukin-1 receptors with N and L6. Plant Cell 9:879-894
66. Parker JE, Holub EB, Frost LN, Falk A, GunnND, Daniels MJ. 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8:2033-2046
67. Qutob D, Tedman-Jones J, Dong S, Kuflu K, Pham H, et al. 2009. Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS ONE 4:e5066
68. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, et al. 2005. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839-1850
69. Rehmany AP, Grenville LJ, Gunn ND, Allen RL, Paniwnyk Z, et al. 2003. A genetic interval and physical contig spanning the Peronospora parasitica (At) avirulence gene locus ATR1Nd. Fungal Genet. Biol. 38:33-42
70. 2 isolate of Peronospora parasitica map to regions known to contain other RPP recognition specificities. Mol. Plant-Microbe Interact. 9:464-473
71. Rentel MC, Leonelli L, Dahlbeck D, Zhao B, Staskawicz BJ. 2008. Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc. Natl. Acad. Sci. USA 105:1091-1096
72. Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL. 2004. The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517-1527
73. Scofield SR, Tobias CM, Rathjen JP, ChangJH, Lavelle DT, et al. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063-2065
74. Sinapidou E, Williams K, Nott L, Bahkt S, Tor M, et al. 2004. Two TIR: NB : LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38:898-909
75. Slusarenko AJ, Schlaich NL. 2003. Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol. Plant Pathol. 4:159-170
76. Sohn KH, Lei R, Nemri A, Jones JDG. 2007. The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19:4077-4090
77. Soylu EM, Soylu S. 2003. Light and electron microscopy of the compatible interaction between Arabidopsis and the downy mildew pathogen Peronospora parasitica. J. Phytopathol. 151:300-306
78. Takahashi H, Miller J, Nozaki Y, Sukamto, Takeda M, et al. 2002. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32:655-667
79. Tang XY, Frederick RD, Zhou JM, Halterman DA, Jia YL, Martin GB. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2063
80. TorM, Holub EB, Brose E, Musker R, Gunn N, et al. 1994. Map positions of 3 loci in Arabidopsis thaliana associated with isolate specific recognition of Peronospora parasitica (downy mildew). Mol. Plant-Microbe Interact. 7:214-222
81. van der Biezen EA, Freddie CT, KahnK, Parker JE, Jones JDG. 2002. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signaling components. Plant J. 29:439-451
82. van der Biezen EA, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-456
83. Van der Hoorn RAL, De WitPJGM,JoostenMHAJ. 2002. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7:67-71
84. van der Hoorn RAL, Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009-2017
85. van Poppel PMJA, GuoJ, van de Vondervoort PJI, JungMWM, Birch PRJ, et al. 2008. The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Mol. Plant-Microbe Interact. 21:1460-1470
86. Vleeshouwers VGAA, Rietman H, Krenek P, Champouret N, Young C, et al. 2008. Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS ONE 3:e2875
87. Voegele RT, Mendgen K. 2003. Rust haustoria: nutrient uptake and beyond. New Phytol. 159:93-100
88. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115-118
89. Win J, Morgan W, Bos J, Krasileva KV, Cano LM, et al. 2007. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349-2369