Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust

Functional Plant Biology

Volumn 36, Issue 5, 2009, Pages 395-408

  Dodds, Peter ^a   Thrall, Peter ^a  

^a CSIRO   (Australia)

Author keywords

Avirulence; Innate immunity; NB LRR.

Indexed keywords

AVIRULENCE; CELLULAR INTERACTION; CO-EVOLUTION; CO-EVOLUTIONARY; COMPLEX INTERACTION; GENE PRODUCTS; GENE RESISTANCE; HOST-PATHOGEN INTERACTIONS; INNATE IMMUNITY; NATURAL ENVIRONMENTS; NB-LRR.; PATHOGEN POPULATIONS; PATHOGENIC ORGANISMS; PLANT RESISTANCE; PLANT-PATHOGEN INTERACTIONS; SPATIO-TEMPORAL SCALE; VIRULENCE GENE;

FLAX; GENES; LINEN; YARN;

PATHOGENS;

COEVOLUTION; HOST-PATHOGEN INTERACTION; RECOGNITION; RUST DISEASE;

LINUM USITATISSIMUM; MELAMPSORA LINI;

EID: 67449131742     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP08320     Document Type: Article

References (93)

1. Akira S (2003) Mammalian Toll-like receptors. Current Opinion in Immunology 15,5-11. doi: 10.1016/S0952-7915(02)00013-4
2. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL (2004) Host-parasite co-evolutionary con?ict between Arabidopsis and downy mildew. Science 306, 1957-1960. doi: 10.1126/science.1104022
3. Anderson PA, Lawrence GJ,Morrish BC, AyliffeMA, Finnegan EJ, Ellis JG (1997) Inactivation of the ?ax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. The Plant Cell 9, 641-651.
4. Armstrong MR, Whisson SC, Pritchard L, Bos JI, 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. Proceedings of the National Academy of Sciences of the United States of America 102, 7766-7771. doi: 10.1073/pnas.0500113102
5. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-speci?ed resistance in Arabidopsis is coupled to AvrRpt2-directed elimination of RIN4. Cell 112, 369-377. doi: 10.1016/S0092-8674(03)00036-9
6. Barrett LG, Thrall PH, Burdon JJ (2007) Evolutionary diversi?cation through hybridization in a wild host-pathogen interaction. Evolution 61, 1613-1621. doi: 10.1111/j.1558-5646.2007.00141.x
7. Barrett LG, Thrall PH, Burdon JJ, Linde C (2008a) Pathogen life-history and the evolutionary potential of populations. Trends in Ecology & Evolution 23, 678-685. doi: 10.1016/j.tree.2008.06.017
8. Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC (2008b) Population Structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Molecular Ecology 17, 3401-3415. doi: 10.1111/j.1365-294X.2007.03503.x
9. Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292, 2281-2285. doi: 10.1126/science. 1061337
10. Bhattacharjee S, Hiller NL, Liolio K, Win J, Kanneganti T-D, Young C, amoun S, Haldar K (2006) The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens 2, e50.doi: 10.1371/journal.ppat.0020050
11. Birch PRJ, 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. doi: 10.1016/j.pbi.2008.04.005
12. Burdon JJ (1994) The distribution and origin of genes for race speci?c resistance to Melampsora lini in Linum marginale. Evolution 48, 1564-1575.
13. Burdon JJ (1997) The evolution of gene-for-gene interactions in natural pathosystems. In 'The gene-for-gene relationship in plant-parasite interactions'. (Eds IR Crute, EB Holub, JJ Burdon) pp. 245-262. (CAB International: Wallingford, UK)
14. Burdon JJ, Jarosz AM (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: I. Patterns of resistance and racial variation in a large host population. Evolution 45, 205-217. doi: 10.2307/2409494
15. Burdon JJ, Roberts JK (1995) The population genetic Structure of the rust fungus Melampsora lini as revealed by pathogenicity, isozyme and RFLP markers. Plant Pathology 44, 270-278. doi: 10.1111/j.1365-3059. 1995.tb02778.x
16. Burdon JJ, Thompson JN (1995) Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. Journal of Ecology 83, 199-206. doi: 10.2307/2261558
17. Burdon JJ, Thrall PH (2000) Co-evolution at multiple spatial scales: Linum marginale-Melampsora lini from the individual to the species. Evolutionary Ecology 14, 261-281. doi: 10.1023/A:1011042721274
18. Burdon JJ, Thrall PH, Brown AHD (1999) Resistance and virulence Structure in two Linum marginale - Melampsora lini host-pathogen metapopulations with different mating systems. Evolution 53, 704-716. doi: 10.2307/2640711
19. Burdon JJ, Thrall PH, Lawrence GJ (2002) Co-evolutionary patterns in the Linum marginale-Melampsora lini association at a continental scale. Canadian Journal of Botany 80, 288-296. doi: 10.1139/b02-007
20. BüttnerD,BonasU(2003)Common strategies of plant and animal pathogenic bacteria. Current Opinion in Plant Biology 6, 312-319. doi: 10.1016/S1369-5266(03)00064-5
21. Catanzariti A-M, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from?ax rust are highly enriched for avirulence elicitors. The Plant Cell 18, 243-256. doi: 10.1105/tpc.105.035980
22. Catanzariti A-M, Dodds PN, Ellis JG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiology Letters 269, 181-188. doi: 10.1111/j.1574-6968.2007.00684.x
23. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814. doi: 10.1016/j.cell.2006.02.008
24. Dangl JL, Jones JDG(2001)Plant pathogens and integrated defence responses to infection. Nature 411, 826-833. doi: 10.1038/35081161
25. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (2003) Physical interaction between RRS1-R-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences of the United States of America 100, 8024-8029. doi: 10.1073/pnas.1230660100
26. Dodds PN, Lawrence GJ, Pryor AJ, Ellis JG (2000) Genetic analysis and evolution of plant disease resistance genes. In 'Molecular plant pathology'. (Eds M Dickinson, J Beynon) pp. 88-107. (Shef?eld Academic Press: Shef?eld, UK)
27. Dodds PN, Lawrence GJ, Ellis JG (2001a) Contrasting modes of evolution acting on the complex N locus for rust resistance in fax. The Plant Journal 27, 439-453. doi: 10.1046/j.1365-313X.2001.01114.x
28. Dodds PN, Lawrence GJ, Pryor AJ, Ellis JG (2001b) Six amino acid changes con?ned to the leucine-rich repeat b-strand/b-turn motif determine the difference between the P and P2 rust resistance speci?cities in fax. The Plant Cell 13, 163-178.
29. Dodds PN, Lawrence GJ, Catanzariti A-M, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. The Plant Cell 16, 755-768. doi: 10.1105/tpc.020040
30. Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang CA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specifcity and co-evolution of the fax resistance genes and fax rust avirulence genes. Proceedings of the National Academy of Sciences of the United States of America 103, 8888-8893. doi: 10.1073/pnas.0602577103
31. Panstruga R, Dodds PN (2009) Terri?c protein traf?c: the mystery of how ?lamentous pathogens deliver effectors into host plant cells. Science, in press.
32. Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, Tyler BM (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen encoded machinery. The Plant Cell 20, 1930-1947. doi: 10.1105/tpc.107.056093
33. Ellis JG, Dodds PN (2003) Plant disease resistance: monitoring a pathogen targeted host protein. Current Biology 13, R400-R402. doi: 10.1016/S0960-9822(03)00321-X
34. Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identi?cation of regions in alleles of the ?ax rust resistance gene L that determine differences in gene-for-gene speci?city. The Plant Cell 11, 495-506.
35. Ellis JG, Dodds PN, Lawrence GJ (2007) The role of secreted proteins in diseases of plants caused by rusts, powdery mildew and smut fungi. Current Opinion in Microbiology 10, 326-331. doi: 10.1016/j.mib.2007.05.015
36. Endo T, Ikeo K, Gojobori T (1996) Large scale search for genes on which positive selection may operate. Molecular Biology and Evolution 13, 685-690.
37. Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275-296. doi: 10.1146/annurev.py.09. 090171.001423
38. Girardin SE, Travassos LH, Nerve M, Blanot D, Boneca IG, Philpott DJ, Sansonetti PJ, Mengin-Lecreulx D (2003) Peptidoglycan molecular requirements allowing detection by Nod 1 and Nod 2. Journal of Biological Chemistry 278, 41702-41708. doi: 10.1074/jbc.M307198200
39. Hahn M, Mendgen K (1992) Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170,95-103. doi: 10.1007/BF01378785
40. Hahn M, Mendgen K (2001) Signal and nutrient exchange at biotrophic plant-fungus interfaces. Current Opinion in Plant Biology 4, 322-327.doi: 10.1016/S1369-5266(00)00180-1
41. Heath MC (1997) Signalling between pathogenic rust fungi and resistant orsusceptible host plants. Annals of Botany 80, 713-720. doi: 10.1006/anbo.1997.0507
42. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estraño C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306, 1934-1937. doi: 10.1126/science.1102737
43. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167-170. doi: 10.1038/335167a0
44. Hwang C-F, Williamson VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signalling by the tomato resistance protein Mi. The Plant Journal 34, 585-593. doi: 10.1046/j.1365-313X.2003.01749.x
45. Jarosz AM, Burdon JJ (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: II Local and regional variation in patterns of resistance and racial Structure. Evolution 45, 1618-1627. doi: 10.2307/2409783
46. Jarosz AM, Burdon JJ (1992) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: III In?uence of pathogen epidemics on host survivorship and fower production. Oecologia 89,53-61. doi: 10.1007/BF00319015
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 Journal 19, 4004-4014. doi: 10.1093/emboj/19.15. 4004
48. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
49. Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44,41-60. doi: 10.1146/annurev.phyto.44.070505.143436
50. Kemen E, Kemen AC, Rafqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identi?cation of a protein from rust fungi transferred from haustoria into infected plant cells. Molecular Plant-Microbe Interactions 18, 1130-1139. doi: 10.1094/MPMI-18-1130
51. Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganisation of microtubules and micro?laments in ?ax cells during the resistance response to ?ax rust infection. Planta 195, 237-247. doi: 10.1007/BF00199684
52. Kobayashi I, Murdoch LJ, Kunoh H, Hardham AR (1995) Cell biology of early events in the resistance response to infection by pathogenic fungi. Canadian Journal of Botany 73, 418-425. doi: 10.1139/b95-278
53. Kobayashi I, Kobayashi Y, Hardham AR (1997) Inhibition of rust-induced hypersensitive response in ?ax cells by themicrotubule inhibitor oryzalin. Australian Journal of Plant Physiology 24, 733-740. doi: 10.1071/PP97060
54. Lawrence GJ, Burdon JJ (1989) Flax rust from L. marginale: variation in a natural host-pathogen interaction. Canadian Journal of Botany 66, 3192-3198.
55. Lawrence GJ, Shepherd KW, Mayo GME (1981) Fine Structure of genes controlling pathogenicity in ?ax rust, Melampsora lini. Heredity 46, 297-313. doi: 10.1038/hdy.1981.42
56. Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for ?ax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2andthetobaccoviral resistancegeneN.The Plant Cell7,1195-1206.
57. Lawrence GJ, Dodds PN, Ellis JG (2007) Rust of ?ax and linseed caused by Melampsora lini. Molecular Plant Pathology 8, 349-364. doi: 10.1111/j.1364-3703.2007.00405.x
58. Lawrence GJ, Anderson PA, Dodds PN, Ellis JG (2009) Relationships between rust resistance genes at the M locus in fax. Molecular Plant Pathology, in press.
59. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG (2000) Regions outside of the leucine-rich repeats of ?ax rust resistance proteins play a role in speci?city determination. The Plant Cell 12, 1367-1378.
60. Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III efector molecules and is required for RPM1-mediated resistance in Arabidopisis. Cell 108, 743-754. doi: 10.1016/S0092-8674(02)00661-X
61. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III effector AvrRpt2 and modulates RPS2- mediated resistance. Cell 112, 379-389. doi: 10.1016/S0092-8674(03) 00040-0
62. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306, 1930-1933. doi: 10.1126/science.1102452
63. Mauricio R, Stahl EA, Korves T, Tian D, Kreitman M, Bergelson J (2003) Natural selection for polymorphism in the disease resistance gene RPS2 of Arabidopsis thaliana. Genetics 163, 735-746.
64. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Research 8, 1113-1130.
65. Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death.EMBO Journal 21, 4511-4519. doi: 10.1093/emboj/cdf453
66. Mondragon-Palomino M, Meyers B, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the coplete NBS-LRR family of Arabidopsis thaliana. Genome Research 12, 1305-1315. doi: 10.1101/gr.159402
67. Murdoch LJ, Hardham AR (1998) Components in the haustorial wall of the ?ax rust fungus, Melampsora lini, are labelled by three anti-calmodulin monoclonal antibodies. Protoplasma 201, 180-193. doi: 10.1007/BF01287414
68. Murdoch LJ, Kobayashi I, Hardham AR (1998) Production and characterisation of monoclonal antibodies to cell wall components of the fax rust fungus. European Journal of Plant Pathology 104, 331-346. doi: 10.1023/A:1008670420652
69. NeiM, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Sciences of the United States of America 94, 7799-7806. doi: 10.1073/pnas.94.15.7799
70. Nurnberger T, Brunner F, Kemmerking B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198, 249-266. doi: 10.1111/j.0105-2896. 2004.0119.x
71. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz BJ, Dixon JE (2000) Disruption of signalling by Yersinia effector YopJ, A ubiquitin-like protein protease. Science 290, 1594-1597. doi: 10.1126/science.290.5496.1594
72. Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Current Opinion in Plant Biology 6, 320-326. doi: 10.1016/S1369-5266(03)00043-8
73. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance speci?cities result from sequence exchange between tandemly repeated gene at the Cf-4/9 locus of tomato. Cell 91, 821-832. doi: 10.1016/S0092-8674(00)80470-5
74. Perfect SE, Green JR (2001) Infection Structures of biotrophic and hemibiotrophic fungal plant pathogens. Molecular Plant Pathology 2, 101-108. doi: 10.1046/j.1364-3703.2001.00055.x
75. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR,Whisson SC, Kamoun S, Tyler BM, Birch PRJ, Beynon JL (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. The Plant Cell 17, 1839-1850. doi: 10.1105/tpc.105.031807
76. ShanW,CaoM,LeungD,TylerBM(2004)TheAvr1b locus ofPhytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions 17, 394-403. doi: 10.1094/MPMI.2004.17.4.394
77. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230-1233. doi: 10.1126/science.1085671
78. Stahl EA, Dwyer G,Mauricio R, KreitmanM, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667-671. doi: 10.1038/23260
79. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE (2001) Common and contrasting themes of plant and animal diseases. Science 292, 2285-2289. doi: 10.1126/science.1062013
80. Thompson JN (1994) 'The co-evolutionary process.' (University of Chicago Press: Chicago, IL)
81. Thompson JN (1999) Speci?c hypotheses on the geographic mosaic of co-evolution. American Naturalist 153,S1-S14. doi: 10.1086/303208
82. Thrall PH, Burdon JJ (2000) Effects of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathology 49, 767-773. doi: 10.1046/j.1365-3059.2000.00523.x
83. Thrall PH, Burdon JJ (2003) Evolution of virulence in a plant host-pathogen metapopulation. Science 299, 1735-1737. doi: 10.1126/science.1080070
84. Thrall PH,Burdon JJ,YoungAG(2001)Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. Journal of Ecology 89, 736-748.
85. Thrall PH, Burdon JJ, Bever JD (2002) Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56, 1340-1351.
86. Tyler BM (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cellular Microbiology 11,13-20. doi: 10.1111/j.1462-5822.2008.01240.x
87. UedaH,YamaguchiY, SanoH(2006)Direct Interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Molecular Biology 61,31-45. doi: 10.1007/s11103-005-5817-8
88. van derHoorn RAL,Kamoun S (2008) Fromguard to decoy: a newmodel for perception of plant pathogen effectors. The Plant Cell 20, 2009-2017. doi: 10.1105/tpc.108.060194
89. van der Hoorn RAL, de Wit PJGM, Joosten MHAJ (2002) Balancing selection favors guarding resistance proteins. Trends in Plant Science 7,67-71. doi: 10.1016/S1360-1385(01)02188-4
90. Voegele RT,Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytologist 159,93-100. doi: 10.1046/j.1469-8137.2003.00761.x
91. Wang C-IA, Guncar G, Forwood JK, Teh T, Catanzariti A-M, et al. (2007) Crystal Structures of ?ax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for ?ax disease resistance speci?city. The Plant Cell 19, 2898-2912. doi: 10.1105/tpc.107.053611
92. 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. doi: 10.1038/nature06203
93. White SN, Taylor KH, Abbey CA, Gill CA, Womack JE (2003) Haplotype variation in bovine Toll-line receptor 4 and computational prediction of a positively selected ligand-binding domain. Proceedings of the National Academy of Sciences of the United States of America 100, 10364-10369. doi: 10.1073/pnas.1333957100