Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi

Molecular Ecology

Volumn 20, Issue 7, 2011, Pages 1492-1507

  Kiss, Levente ^a   Pintye, Alexandra ^a   KovÁcs, Gábor M ^a,b   Jankovics, Tünde ^a   Fontaine, Michael C ^c   Harvey, Nick ^d   Xu, Xiangming ^e   Nicot, Philippe C ^f   Bardin, Marc ^f   Shykoff, Jacqui A ^c   Giraud, Tatiana ^c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c UNIVERSITÉ PARIS SUD   (France)

^d Genetic Marker Services   (United Kingdom)

^e EAST MALLING RESEARCH   (United Kingdom)

^f INRA   (France)

Author keywords

biotrophic pathogens; isolation in time; speciation; tri trophic interactions

Indexed keywords

AMPELOMYCES; ERYSIPHALES; FUNGI; MALUS X DOMESTICA; PODOSPHAERA LEUCOTRICHA;

EID: 79953060752     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05007.x     Document Type: Article

References (68)

1. Agapow P-M, Burt A, (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101-102. (Pubitemid 33691862)
2. Berlocher SH, Feder JL, (2002) Sympatric speciation in phytophagous insects: moving beyond controversy. Annual Review of Entomology, 47, 773-815. (Pubitemid 34108596)
3. Burt A, Carter DA, Koenig GL, White TJ, Taylor JW, (1996) Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proceedings of the National Academy of Sciences of the USA, 93, 770-773. (Pubitemid 26041166)
4. Cavalli-Sforza LL, Edwards AWF, (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233-257.
5. Chessel D, Dufour AB, Thiouluose J, (2004) The ade4 package-I: one-table methods. R News, 4, 5-10.
6. Corpet F, (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research, 16, 10881-10890.
7. Coyne JA, Orr HA, (2004) Speciation. Sinauer Associates, Sunderland, MA.
8. Devaux C, Lande R, (2008) Incipient allochronic speciation due to non-selective assortative mating by flowering time, mutation, and genetic drift. Proceedings of the Royal Society of London, Series B, 275, 2723-2732.
9. Dutech C, Enjalbert J, Fournier E, et al. (2007) Challenges of microsatellite isolation in fungi. Fungal Genetics & Biology, 44, 933-949. (Pubitemid 47334889)
10. Falk SP, Gadoury DM, Cortesi P, Pearson RC, Seem RC, (1995) Parasitism of Uncinula necator ascomata by the mycoparasite Ampelomyces quisqualis. Phytopathology, 85, 794-800.
11. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG, (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. Journal of Bacteriology, 186, 1518-1530. (Pubitemid 38248742)
12. Filatov DA, (2002) ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Molecular Ecology Notes, 2, 621-624. (Pubitemid 35436767)
13. Fisher MC, Hanage WP, de Hoog S, et al. (2005) Low effective dispersal of asexual genotypes in heterogeneous landscapes by the endemic pathogen Penicillium marneffei. PLoS Pathogens, 1 (2), e20.
14. Fontaneto D, Herniou EA, Boschetti C, et al. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5 (4), e87.
15. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113-118.
16. Gavrilets S, (2004) Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, NJ.
17. Gavrilets S, Losos JB, (2009) Adaptive radiation: contrasting theory with data. Science, 323, 732-737.
18. Giraud T, (2004) Patterns of within population dispersion and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia. Heredity, 95, 559-565. (Pubitemid 39606218)
19. Giraud T, (2006a) Selection against migrant pathogens: the immigrant inviability barrier in pathogens. Heredity, 97, 316-318. (Pubitemid 44639516)
20. Giraud T, (2006b) Speciation in parasites: host switching does not automatically lead to allopatry. Trends in Parasitology, 22, 151-152.
21. Giraud T, Villaréal L, Austerlitz F, Le Gac M, Lavigne C, (2006) Importance of the life cycle in host race formation and sympatric speciation in parasites. Phytopathology, 96, 280-287.
22. Giraud T, Enjalbert J, Fournier E, Delmotte F, Dutech C, (2008a) Population genetics of fungal diseases of plants. Parasite, 15, 449-454.
23. Giraud T, Refrégier G, de Vienne DM, Le Gac M, Hood ME, (2008b) Speciation in fungi. Fungal Genetics & Biology, 45, 791-802.
24. Giraud T, Gladieux P, Gavrilets S, (2010) Linking emerging diseases and speciation. Trends in Ecology and Evolution, 25, 387-395.
25. Glawe DA, (2008) The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology, 46, 27-51.
26. Hardy OJ, Vekemans X, (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual of population levels. Molecular Ecology Notes, 2, 618-620. (Pubitemid 35436766)
27. Harvey NG, (2006) Characterization of six polymorphic microsatellite loci from Ampelomyces quisqualis, intracellular mycoparasite and biocontrol agent of powdery mildew. Molecular Ecology Notes, 6, 1188-1190. (Pubitemid 44807981)
28. Hendry AP, Day T, (2005) Population structure attributable to reproductive date: isolation-by-time and adaptation-by-time. Molecular Ecology, 14, 901-916. (Pubitemid 40466224)
29. Holb IJ, (2005) Effect of pruning on disease incidence of apple scab and powdery mildew in integrated and organic apple production. International Journal of Horticultural Science, 11, 57-61.
30. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267. (Pubitemid 43100040)
31. Johnson PA, Hoppensteadt FC, Smith JJ, Bush GL, (1996) Conditions for sympatric speciation: a diploid model incorporating habitat fidelity and non-habitat assortative mating. Evolutionary Ecology, 10, 187-205.
32. Jombart T, (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405. (Pubitemid 351737150)
33. Kiss L, (1998) Natural occurrence of Ampelomyces mycoparasites in mycelia of powdery mildew fungi. New Phytologist, 140, 709-714. (Pubitemid 29066977)
34. Kiss L, (2001) The role of hyperparasites in host plant-parasitic fungi relationships. In: Biotic Interactions in Plant-Pathogen Associations (eds, Jeger MJ, Spence NJ,), pp. 227-236. CABI, Wallingford.
35. Kiss L, (2008) Intracellular mycoparasites in action: interactions between powdery mildew fungi and Ampelomyces. In: Stress in Yeasts and Filamentous Fungi (eds, Avery SV, Stratford M, Van West P,), pp. 37-52. Academic Press, Elsevier, London.
36. Kiss L, Nakasone KK, (1998) Ribosomal DNA internal transcribed spacer sequences do not support the species status of Ampelomyces quisqualis, a hyperparasite of powdery mildew fungi. Current Genetics, 33, 362-367. (Pubitemid 28297113)
37. Kiss L, Russell JC, Szentiványi O, Xu X, Jeffries P, (2004) Biology and biocontrol potential of Ampelomyces mycoparasites, natural antagonists of powdery mildew fungi. Biocontrol Science & Technology, 14, 635-651. (Pubitemid 38893715)
38. Kondrashov AS, Mina MV, (1986) Sympatric speciation: when is it possible? Biological Journal of the Linnean Society, 27, 201-223.
39. Le Gac M, Giraud T, (2008) Existence of a pattern of reproductive character displacement in Basidiomycota but not in Ascomycota. Journal of Evolutionary Biology, 21, 761-772. (Pubitemid 351521539)
40. Legendre P, Legendre L, (1998) Numerical Ecology. Developments in Environmental Modelling, 20. Elsevier, Amsterdam
41. Levene H, (1953) Genetic equilibrium when more than one ecological niche is available. American Naturalist, 87, 331-333.
42. Liang C, Yang J, Kovács GM, Szentiványi O, Li B, et al. (2007) Genetic diversity of Ampelomyces mycoparasites isolated from different powdery mildew fungi in China inferred from analyses of rDNA ITS sequences. Fungal Diversity, 24, 225-240.
43. Loiselle BA, Sork VL, Nason J, Graham C, (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany, 82, 1420-1425. (Pubitemid 3002677)
44. de Meeûs T, Michalakis Y, Renaud F, (1998) Santa Rosalia revisited: or why are there so many kinds of parasites in 'The garden of earthly delights?' Parasitology Today, 14, 10-13. (Pubitemid 28108822)
45. Montarry J, Cartolaro P, Delmotte F, Jolivet J, Willocquet L, (2008) Genetic structure and aggressiveness of Erysiphe necator populations during grapevine powdery mildew epidemics. Applied and Environmental Microbiology, 74, 6327-6332.
46. Montarry J, Cartolaro P, Richard-Cervera S, Delmotte F, (2009) Spatio-temporal distribution of Erysiphe necator genetic groups and their relationship with disease levels in vineyards. European Journal of Plant Pathology, 123, 61-70.
47. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH, (2008) Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evolutionary Bioinformatics, 4, 193-201. (Pubitemid 351865649)
48. Nischwitz C, Newcombe G, Anderson CL, (2005) Host specialization of the mycoparasite Eudarluca caricis and its evolutionary relationship to Ampelomyces. Mycological Research, 109, 421-428. (Pubitemid 40623428)
49. Park M-J, Choi Y-J, Hong S-B, Shin H-D, (2010) Genetic variability and mycohost association of Ampelomyces quisqualis isolates inferred from phylogenetic analyses of ITS rDNA and actin gene sequences. Fungal Biology, 114, 235-247.
50. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
51. Savolainen V, Anstett M-C, Lexer C, et al. (2006) Sympatric speciation in palms on an oceanic island. Nature, 441, 210-213.
52. Seifert KA, Wingfield BD, Wingfield MJ, (1995) A critique of DNA sequence analysis in the taxonomy of filamentous Ascomycetes and ascomycetous anamorphs. Canadian Journal of Botany, 73 (Suppl. 1), S760-S767.
53. Spratt BG, Hanage WP, Li B, Aanensen DM, Feil EJ, (2004) Displaying the relatedness among isolates of bacterial species-the eBURST approach. FEMS Microbiology Letters, 241, 129-134. (Pubitemid 39642986)
54. Staden R, Beal KF, Bonfield JK, (2000) The Staden package, 1998. Methods in Molecular Biology, 132, 115-130.
55. Stamm P, (1983) The evolution of reproductive isolation in closely adjacent plant populations through differential flowering time. Heredity, 50, 105-118.
56. Sullivan RF, White Jr JF, (2000) Phoma glomerata as a mycoparasite of powdery mildew. Applied and Environmental Microbiology, 66, 425-427. (Pubitemid 30030551)
57. Swofford DL, (2003). PAUP*. Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.
58. Szentiványi O, Kiss L, (2003) Overwintering of Ampelomyces mycoparasites on apple trees and other plants infected with powdery mildews. Plant Pathology, 53, 737-746. (Pubitemid 38051327)
59. Szentiványi O, Kiss L, Russell JC, et al. (2005) Ampelomyces mycoparasites from apple powdery mildew identified as a distinct group based on single-stranded conformation polymorphism analysis of the rDNA ITS region. Mycological Research, 109, 429-438. (Pubitemid 40623429)
60. Sztejnberg A, Galper S, Mazar S, Lisker N, (1989) Ampelomyces quisqualis for biological and integrated control of powdery mildew in Israel. Journal of Phytopathology, 124, 285-295.
61. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. (Pubitemid 47236692)
62. Taylor JW, (1999) The evolution of asexual fungi. Annual Review of Phytopathology, 37, 197-246.
63. Théron A, Combes C, (1995) Asynchrony of infection timing, habitat preference, and sympatric speciation of schistosome parasites. Evolution, 49, 372-375.
64. Thomas Y, Bethenoda M-T, Pelozuelo L, Frérot B, Bourguet D, (2003) Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hubner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution, 57, 261-273. (Pubitemid 36333337)
65. Turner KME, Hanage WP, Fraser C, Connor TR, Spratt BG, (2007) Assessing the reliability of eBURST using simulated populations with known ancestry. BMC Microbiology, 7, 30.
66. Van Putten WF, Elzinga JA, Biere A, (2007) Host fidelity of the pollinator guilds of Silene dioica and S. latifolia: possible consequences for sympatric host race differentiation of a vectored plant disease. International Journal of Plant Science, 168, 421-434. (Pubitemid 46668616)
67. Vekemans X, Hardy OJ, (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology, 13, 921-935. (Pubitemid 38390597)
68. de Vienne DM, Refrégier G, Hood ME, et al. (2009) Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. Journal of Evolutionary Biology, 22, 683-698.