Diversity and evolution of effector loci in natural populations of the plant pathogen melampsora lini

Molecular Biology and Evolution

Volumn 26, Issue 11, 2009, Pages 2499-2513

  Barrett, Luke G ^a,b,c   Thrall, Peter H ^a   Dodds, Peter N ^a   Van Der Merwe, Marlien ^a,d   Linde, Celeste C ^b   Lawrence, Gregory J ^a   Burdon, Jeremy J ^a  

^a CSIRO   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c UNIVERSITY OF CHICAGO   (United States)

^d ROYAL BOTANIC GARDENS AND DOMAIN TRUST   (Australia)

Author keywords

Effector; Metapopulation; Parasite; Polymorphism; Selection; Virulence

Indexed keywords

NUCLEOTIDE; FUNGAL PROTEIN;

ARTICLE; BACTERIUM TRANSFORMATION; CONTROLLED STUDY; GENE FREQUENCY; GENE LOCUS; GENETIC RESISTANCE; GENETIC SELECTION; GENETIC VARIABILITY; HAPLOTYPE; HOST PATHOGEN INTERACTION; LINSEED; MELAMPSORA LINI; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT COMMUNITY; PLANT DISEASE; PLANT PARASITIC PLANT DISEASE; RHIZOBIUM; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION; VIRULENCE; WILD TYPE; BASIDIOMYCETES; CLASSIFICATION; FLAX; GENETIC POLYMORPHISM; GENETICS; MICROBIOLOGY; PHYSIOLOGY; PLANT;

AGROBACTERIUM; LINUM MARGINALE; LINUM USITATISSIMUM; MELAMPSORA LINI;

BASIDIOMYCOTA; EVOLUTION, MOLECULAR; FLAX; FUNGAL PROTEINS; GENETIC VARIATION; PLANTS; POLYMORPHISM, GENETIC;

EID: 73349090580     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp166     Document Type: Article

References (84)

1. Alfano JR, Collmer A. 2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopath. 42:385-414.
2. Anderson RM, May RM. 1982. Coevolution of hosts and parasites. Parasitology. 85:411-426.
3. Antonovics J, Thrall PH. 1994. Cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc R Soc Lond B. 257:105-110.
4. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW. 2004. Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell. 16:309-318.
5. Ayliffe MA, Dodds PN, Lawrence GJ. 2001. Characterisation of a b-tubulin gene from Melampsora lini and comparison of fungal b-tubulin genes. Mycol Res. 105:818-826.
6. Barrett LG, Thrall PH, Burdon JJ. 2007. Evolutionary diversification through hybridization in a wild host-pathogen interaction. Evolution. 61:1613-1621.
7. Barrett LG, Thrall PH, Burdon JJ, Linde CC. 2008. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol. 23: 678-685.
8. Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC. 2008. Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Mol Ecol. 17:3401-3415.
9. Bergelson J, Kreitman M, Stahl EA, Tian DC. 2001. Evolutionary dynamics of plant R-genes. Science. 292:2281-2285.
10. Brown JKM, Hovmoller MS. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science. 297:537-541.
11. Buitkamp J, Filmether P, Stear MJ, Epplen JT. 1996. Class I and class II major histocompatibility complex alleles are associated with faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Parasitol Res. 82:693-696.
12. Burdon JJ. 1992. Host population subdivision and the genetic structure of natural pathogen populations. Adv Plant Path. 8:81-94.
13. Burdon JJ. 1994. The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale. Evolution. 48:1564-1575.
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.
15. Burdon JJ, Jarosz AM. 1992. Temporal variation in the racial structure of flax rust (Melampsora lini) populations growing on natural stands of wild flax (Linum marginale): local versus metapopulation dynamics. Plant Pathol. 41:165-179.
16. Catanzariti AM, Dodds PN, Ellis JG. 2007. Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett. 269:181-188.
17. Catanzariti A-M, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell. 18:243-256.
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. Clarke B. 1976. The ecological genetics of host-parasite relationships. In: Taylor ER, Muller R, editors. Genetic aspects of host-parasite relationships. Oxford: Blackwell Scientific.
20. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defence response to pathogens. Nature. 411:826-833.
21. 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.
22. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, Ayliffe MA, Kobe B, Ellis JG. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolu-tion of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA. 103:8888-8893.
23. Flor HH. 1955. Host-parasite interaction in flax rust-its genetics and other implications. Phytopathology. 45:680-685.
24. Ford MJ. 2002. Applications of selective neutrality tests to molecular ecology. Mol Ecol. 11:1245-1262.
25. Friesen TL, Stukenbrock EH, Liu ZH, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet. 38:953-956.
26. Gabriel DW. 1999. Why do pathogens carry avirulence genes? Physiol Mol Plant Pathol. 55:205-214.
27. Gandon S. 1998. Local adaptation and host-parasite interactions. Trends Ecol Evol. 13:214-216.
28. Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc Lond B. 263: 1003-1009.
29. Gillespie JH. 1975. Natural selection for resistance to epidemics. Ecology. 56:493-495.
30. Gonzalez E, Dhanda R, Bamshad M, et al. (15 co-authors). 2001. Global survey of genetic variation in CCR5, RANTES, and MIP-1a: impact on the epidemiology of the HIV-1 pandemic. Proc Nat Acad Sci USA. 98:5199-5204.
31. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 41:95-98.
32. Hedrick PW. 1974. Genetic variation in a heterogeneous environment. I. Temporal heterogeneity and the absolute dominance model. Genetics. 78:757-770.
33. Hedrick PW. 2006. Genetic polymorphism in heterogeneous environments: the age of genomics. Ann Rev Ecol Evol Syst. 37:67-93.
34. 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.
35. Jarosz AM, Burdon JJ. 1992. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: III. influence of pathogen epidemics on host survivorship and flower production. Oecologia. 89:53-61.
36. Jayakar SD. 1970. A mathematical model for interaction of gene frequencies in a parasite and its host. Theor Pop Biol. 1:140-164.
37. Kniskern J, Rausher MD. 2001. Two modes of host-enemy coevolution. Popul Ecol. 43:3-14.
38. Kruijt M, Kip DJ, Joosten M, Brandwagt BF, de Wit P. 2005. The Cf-4 and Cf-9 resistance genes against Cladosporium fulvum are conserved in wild tomato species. Mol PlantMicrobe Interact. 18:1011-1021.
39. Laine AL, Tellier A. 2008. Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos. 117:1281-1288.
40. Lawrence GJ. 1989. Flax rust from Linum marginale pathogenicity reactions on the Linum usitatissimum set of differential varieties. Can J Bot. 67:3187-3191.
41. Lawrence GJ, Burdon JJ. 1989. Flax rust from Linum margin-ale\variation in a natural host pathogen interaction. Can J Bot. 67:3192-3198.
42. Lawrence GJ, Dodds PN, Ellis JG. 2007. Rust of flax and linseed caused by Melampsora lini. Mol Plant Path. 8:349-364.
43. Lawrence GJ, Mayo GME, Sheperd KW. 1981. Interactions between genes controlling pathogenicity in the flax rust fungus. Genetics. 71:12-19.
44. Lockett SF, Robertson JR, Brettle RP, Yap PL, Middleton D, Brown AJL. 2001. Mismatched human leukocyte antigen alleles protect against heterosexual HIV transmission. JAIDS. 27:277-280.
45. Ma WB, Dong FFT, Stavrinides J, Guttman DS. 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. Plos Genet. 2:2131-2142.
46. Mantel N. 1967. The detection of disease clustering and a generalised regression approach. Cancer Res. 27:209-220.
47. Martin D, Rybicki E. 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 16:562-563.
48. Martin DP, Williamson C, Posada D. 2005. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics. 21:260-262.
49. McDill J, Repplinger M, Simpson BB, Kadereit JW. 2009. The phylogeny of Linum and Linaceae subfamily Linoideae, with implications for their systematics, biogeography, and evolution of heterostyly. Syst Bot. 34:386-405.
50. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 351:652-654.
51. Nei M. 1987. Molecular evolutionary genetics. New York: Columbia University Press.
52. Nielsen R, Yang ZH. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 148:929-936.
53. Ong LE, Innes RW. 2006. AvrB mutants lose both virulence and avirulence activities on soybean and Arabidopsis. Mol Microbiol. 60:951-962.
54. Padidam M, Sawyer S, Fauquet CM. 1999. Possible emergence of new geminiviruses by frequent recombination. Virology. 265:218-225.
55. Paterson S, Wilson K, Pemberton JM. 1998. Major histocompat-ibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc Natl Acad Sci USA. 95:3714-3719.
56. Peakall R, Smouse PE. 2005. GenAlEx v6: genetic analysis in Excel. Canberra (Australia): Australian National University.
57. Piertney SB, Oliver MK. 2006. The evolutionary ecology of the major histocompatibility complex. Heredity. 96:7-21.
58. Posada D, Crandall KA. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA. 98:13757-13762.
59. Prentice MB, James KD, Parkhill J, et al. (15 co-authors). 2001. Yersinia pestis pFra shows biovar-specific differences and recent common ancestry with a Salmonella enterica serovar typhi plasmid. J Bacteriol. 183:2586-2594.
60. Rand DM, Kann LM. 1996. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice and humans. Mol Biol Evol. 13: 735-748.
61. Roy BA, Kirchner JW. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution. 54:51-63.
62. Rozas J, Rozas R. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 15:174-175.
63. Salminen M, Carr JK, Burke DS, McCutchan FE. 1995. Identification of recombination breakpoints in Hiv-1 by bootscanning. Aids Res Hum Retrovir. 11:S119.
64. Sarkar SF, Gordon JS, Martin GB, Guttman DS. 2006. Comparative genomics of host-specific virulence in Pseudo-monas syringae. Genetics. 174:1041-1056.
65. Smith JM. 1992. Analyzing the mosaic structure of genes. J Mol Evol. 34:126-129.
66. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 21:456-463.
67. Swofford DL. 2001. PAUP*, Phylogenetic analysis using parsimony (*and other methods). Sunderland (MA): Sinauer Associates.
68. Tellier A, Brown JKM. 2007. Stability of genetic polymorphism in host-parasite interactions. Proc R Soc Lond B. 274:809-817. (Pubitemid 47056760)
69. Thompson JN. 2005. The geographic mosaic of coevolution. Chicago: The University of Chicago Press.
70. Thrall PH, Burdon JJ. 2000. Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathol. 49:767-773.
71. Thrall PH, Burdon JJ. 2002. Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51:169-184.
72. Thrall PH, Burdon JJ. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science. 299:1735-1737.
73. Thrall PH, Burdon JJ, Bever JD. 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution. 56:1340-1351.
74. Tiffin P, Moeller DA. 2006. Molecular evolution of plant immune system genes. Trend Genet. 22:662-670.
75. van der Merwe MM, Kinnear MW, Barrett LG, Dodds PN, Ericson L, Thrall PH, Burdon JJ. 2009. Positive selection in AvrP4 avirulence gene homologues across the genus Melampsora. Proc R Soc Lond B. 276:2913-2922.
76. Wang CIA, Guncar G, Forwood JK, et al. (12 co-authors). 2007. Crystal structures of flax rust avirulence proteins AvrL567-A and-D reveal details of the structural basis for flax disease resistance specificity. Plant Cell. 19:2898-2912.
77. White TJ, Lee S, Bruns TD, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego (CA): Academic Press.
78. Wichmann G, Ritchie D, Kousik CS, Bergelson J. 2005. Reduced genetic variation occurs among genes of the highly clonal plant pathogen Xanthomonas axonopodis pv. vesicatoria, including the effector gene avrBs2. Appl Environ Microbiol. 71:2418-2432.
79. Williams-Blangero S, McGarvey ST, Subedi J, Wiest PM, Upadhayay RP, Rai DR, Jha B, Olds GR, Wu GL, Blangero J. 2002. Genetic component to susceptibility to Trichuris trichiura: evidence from two Asian populations. Genet Epidemiol. 22:254-264.
80. Yang Z. 1997. PAML: a computer package for phylogenetic analysisbymaximum likelihood. Com AppBiosc. 13:555-556.
81. Yang ZH, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 17:32-43.
82. Yang ZH, Nielsen R, Goldman N, Pedersen AMK. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155:431-449.
83. Yang ZH, Wong WSW, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
84. Zeven AC, Zhokovsky PM. 1975. Dictionary of cultivated plants and their centres of diversity. Wageningen (Netherlands): Centre for Agricultural Publishing and Documentation.