Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Sacristán, Soledad ^a   Vigouroux, Marielle ^a   Pedersen, Carsten ^b   Skamnioti, Pari ^a,d   Thordal Christensen, Hans ^b   Micali, Cristina ^c   Brown, James K M ^a   Ridout, Christopher J ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COEVOLUTION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FUNGAL GENE; GENE SEQUENCE; GENETIC SELECTION; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PLANT FUNGUS INTERACTION; POWDERY MILDEW; RETROPOSON; ASCOMYCETES; BIOLOGICAL MODEL; FUNGAL GENOME; FUNGUS; GENE LIBRARY; GENETICS; LONG INTERSPERSED REPEAT; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT DISEASE; VIRULENCE;

ASCOMYCOTA; ERYSIPHALES; FUNGI;

ASCOMYCOTA; EVOLUTION, MOLECULAR; FUNGI; GENE LIBRARY; GENES, FUNGAL; GENOME, FUNGAL; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MODELS, GENETIC; PHYLOGENY; PLANT DISEASES; PLANTS; RETROELEMENTS; VIRULENCE;

EID: 70449382810     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007463     Document Type: Article

References (63)

1. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329.
2. Ma WB, Guttman DS (2008) Evolution of prokaryotic and eukaryotic virulence effectors. Curr Opin Plant Biol 11: 412-419.
3. Flor HH (1971) Current status of gene for gene concept. Annu Rev Phytopathol 9: 275-296.
4. Alfano JR, Collmer A (2004) Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42: 385-414.
5. Skamnioti P, Ridout CJ (2005) Microbial avirulence determinants: guided missiles or antigenic flak? Mol Plant Pathol 6: 551-559.
6. Sacristán S, García-Arenal F (2008) The evolution of virulence and pathogenicity in plant pathogen populations. Mol Plant Pathol 9: 369-384.
7. Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Crit Rev Plant Sci 13: 97-119.
8. Shen QH, Zhou F, Bieri S, Haizel T, Shirasu K, et al. (2003) Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell 15: 732-744.
9. Brown JKM, Jessop AC (1995) Genetics of avirulences in Erysiphe graminis f. sp. hordei. Plant Pathol 44: 1039-1049.
10. Jensen J, Jensen HP, Jørgensen JH (1995) Linkage studies of barley powdery mildew virulence loci. Hereditas 122: 197-209.
11. Brown JKM (2002) Comparative Genetics of avirulence and fungicide resistance in the powdery mildew fungi. In: Belanger RR, Bushnell WR, Dik AJ, Carver TLW, eds. The Powdery Mildews: a comprehensive treatise. Saint Paul, MN: APS Press. pp 56-66.
12. Skamnioti P, Pedersen C, Al-Chaarani GR, Holefors, A, Thordal-Christensen H, et al. (2008) Genetics of avirulence genes in Blumeria graminis f.sp. hordei and physical mapping of AVRa22 and AVRa12. Fungal Genet Biol 45: 243-252.
13. Marchal E (1902) De la spécialisation du parasitisme chez l' Erysiphe graminis. Compt Rend Acad Sci Paris 135: 210-212.
14. Oku T, Yamashita S, Doi Y, Nishihara N (1985) Host range and forma specialis of cocksfoot powdery mildew fungus (Erysiphe graminis DC) found in Japan. Ann Phytopathol Soc Jpn 51: 613-615.
15. Tosa Y, Matsumura K, Hosaka T (1995) Genetic analysis of interactions between aegilops species and formae speciales of Erysiphe graminis. Jap J Genet 70: 127-134.
16. Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, et al. (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18: 2402-2414.
17. Jiang RHY, Weide R, van de Vondervoort PJI, Govers F (2006) Amplification generates modular diversity at an avirulence locus in the pathogen Phytophthora. Genome Res 16: 827-840.
18. Catanzariti A, Dodds PN, Ellis JG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiol Lett 269: 181-188.
19. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease resistance responses. Science 315: 1098-1103.
20. Zhou E, Jia Y, Singh P, Correll JC, Lee FN (2007) Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet Biol 44: 1024-1034.
21. Kearney B, Ronald PC, Dahlbeck D, Staskawicz BJ (1988) Molecular basis for evasion of plant host defense in bacterial spot disease of pepper. Nature 332: 541-543.
22. Stevens C, Bennett MA, Athanassopoulos E, Tsiamis G, Taylor JD, et al. (1998) Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Mol Microbiol 29: 165-177.
23. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
24. Kulikova T, Akhtar R, Aldebert P, Althorpe N, Andersson M, et al. (2007) EMBL Nucleotide Sequence Database in 2006. Nucleic Acids Res 35: D16-D20.
25. Soanes DM, Talbot NJ (2006) Comparative genomic analysis of phytopathogenic fungi using expressed sequence tag (EST) collections. Mol Plant Pathol 7: 61-70.
26. The UniProt Consortium (2007) The Universal Protein Resource (UniProt). Nucleic Acids Res 36: D190-D195.
27. Rokas A, Carroll SB (2006) Bushes in the tree of life. PLoS Biol 4: e352.
28. Strimmer K, von Haesler A (1997) Likelihood-mapping: A simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci USA 94: 6815-6819.
29. Yang Z, Nielsen R, Goldman N, Petersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
30. 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.
31. Munroe SH (2004) Diversity of antisense regulation in eukaryotes: Multiple mechanisms, emerging patterns. J Cell Biochem 93: 664-671.
32. Hafner MS, Nadler SA (1988) Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332: 258-259.
33. Page RDM, Charleston MA (1998) Trees within trees: phylogeny and historical associations. Trends Ecol Evol 13: 356-359.
34. Charleston MA (1998) Jungles: A new solution to the host/parasite phylogeny reconciliation problem. Math Biosci 149: 191-223.
35. Ronquist F (1995) Reconstructing the history of host-parasite associations using generalised parsimony. Cladistics 11: 73-89.
36. Hughes J, Kennedy M, Johnson KP, Palma RL, Page RDM (2007) Multiple cophylogenetic analyses reveal frequent cospeciation between pelecaniform birds and Pectinopygus lice. Syst Biol 56: 232-251.
37. Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, et al. (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr Opin Plant Biology 11: 373-379.
38. Kvitko BH, Park DH, Velásquez AC, Wei C-F, Russell AB, et al. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5: e1000388.
39. Takamatsu S, Matsuda S (2004) Estimation of molecular clocks for ITS and 28S rDNA in Erysiphales. Mycoscience 45: 340-344.
40. Inuma T, Khodaparast SA, Takamatsu S (2007) Multilocus phylogenetic analyses within Blumeria graminis, a powdery mildew fungus of cereals. Mol Phylogenet Evol 44: 741-751.
41. Lenk A, Thordal-Christensen H (2009) From non-host resistance to lesion mimic mutants - useful for studies of defense signaling. Adv Bot Res. In press.
42. Yahiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47: 85-98.
43. Zohary D, Hopf M (1988) Domestication of Plants in the Old World. Oxford: Clarendon Press. 278 p.
44. Thomas H (1995) Oats. In: Smartt J, Simmonds NW, eds. Evolution of crop plants. 2nd edition. London: Longman. pp. 133-137.
45. Kidwell MG, Lisch DR (2000) Transposable elements and host genome evolution. Trends Ecol Evol 15: 95-99.
46. Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12: 1075-1079.
47. Goodier JL, Kazazian Jr HH (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135: 23-35.
48. Slotkin KR, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285.
49. Khang CH, Park S-Y, Lee Y-H, Valent B, Kang S (2008) Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. MPMI 21: 658-670.
50. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, et al. (2008) Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS ONE 3(6): e2300. doi:10.1371/journal.pone.0002300.
51. Hiura U, Heta H (1955) Studies on the disease-resistance in barley III. Further studies on the physiological races of Erysiphe graminis hordei in Japan. Berichte des Ohara Instituts für Landwirtschaftliche Biologie 10: 135-156.
52. Grell MN, Mouritzen P, Giese H (2004) A Blumeria graminis gene family encoding proteins with a C-terminal variable region with homologues in pathogenic fungi. Gene 311: 181-192.
53. Staden R (1996) The Staden Sequence Analysis Package. Mol Biotechnol 5: 233-241.
54. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
55. Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31: 3537-3539.
56. Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
57. Felsenstein J (1989) PHYLIP - Phylogeny Inference Package (version 3.2). Cladistics 5: 164-166.
58. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
59. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
60. Yang Z (1997) PAML: A program package for phylogenetics analysis by maximum likelihood. CABIOS 13: 555-556.
61. Wong WS, Yang Z, Goldman N, Nielsen R (2004) Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041-1051.
62. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
63. Charleston MA, Robertson DL (2002) Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51: 528-535.