Population structure and temporal maintenance of the multihost fungal pathogen Botrytis cinerea: Causes and implications for disease management

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 1261-1274

  Walker, Anne Sophie ^a   Gladieux, Pierre ^b,c,d   Decognet, Véronique ^e   Fermaud, Marc ^f   Confais, Johann ^a   Roudet, Jean ^f   Bardin, Marc ^e   Bout, Alexandre ^g   C Nicot, Philippe ^e   Poncet, Christine ^g   Fournier, Elisabeth ^h  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ PARIS SUD   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INRA   (France)

^f BORDEAUX SCIENCES AGRO   (France)

^g Institut Sophia Agrobiotech   (France)

^h CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BOTRYOTINIA FUCKELIANA; FUNGI; RUBUS; SOLANUM; VITIS;

MICROSATELLITE DNA;

BOTRYTIS; FRANCE; GENE FLOW; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; HOST RANGE; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; RUBUS; SOLANUM; VITIS;

BOTRYTIS; FRANCE; GENE FLOW; GENETIC VARIATION; GEOGRAPHY; HOST SPECIFICITY; MICROSATELLITE REPEATS; PLANT DISEASES; RUBUS; SOLANUM; VITIS;

EID: 84926292774     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12563     Document Type: Article

References (66)

1. Agapow, P.M., and Burt, A. (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1: 101-102.
2. Albertini, C., Gredt, M., and Leroux, P. (2003) Polymorphism of 14 alpha-demethylase gene (CYP51) in the cereal eyespot fungi Tapesia acuformis and Tapesia yallundae. Eur J Plant Pathol 109: 117-128.
3. Ali, S., Gladieux, P., Rahman, H., Saqib, M.S., Fiaz, M., Ahmad, H., etal. (2013) Inferring the contribution of sexual reproduction, migration and off-season survival to the temporal maintenance of microbial populations: a case study on the wheat fungal pathogen Puccinia striiformis f.sp. tritici. Mol Ecol 23: 603-617.
4. Ali, S., Gladieux, P., Leconte, M., Gautier, A., Justesen, A.F., Hovmøller, M.S., etal. (2014) Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PLoS Pathog 10: e1003903.
5. Amselem, J., Cuomo, C.A., van Kan, J.A.L., Viaud, M., Benito, E.P., Couloux, A., etal. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230. doi:10.1371/journal.pgen.1002230.
6. Beever, R., and Weeds, P. (2004) Taxonomic and genetic variation of Botrytis and Botryotinia. In Botrytis: Biology, Pathology and Control. Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. (eds). Dordrecht, the Netherlands: Kluwer Academic Publisher, pp. 29-52.
7. Beever, R.E., and Parkes, S.L. (2003) Use of nitrate non-utilising (Nit) mutants to determine vegetative compatibility in Botryotinia fuckeliana (Botrytis cinerea). Eur J Plant Pathol 109: 607-613.
8. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., and Bonhomme, F. (1996-2004) Genetix 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier, Montpellier, France. [WWW document]. URL http://www.genetix.univ-montp2.fr/genetix/intro.htm.
9. Boyd-Wilson, K., Obanor, F., Butler, R.C., Harris-Virgin, P., Langford, G.I., Smith, J.T., and Walter, M. (2013) Sources of Botrytis cinerea inoculum for flower infection in blackcurrants in New Zealand. Australas Plant Path 42: 27-32.
10. Brunner, P.C., Torriani, S.F.F., Croll, D., Stukenbrock, E.H., and McDonald, B.A. (2013) Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol Biol Evol 30: 1337-1347.
11. Choquer, M., Fournier, E., Kunz, C., Levis, C., Pradier, J.M., Simon, A., and Viaud, M. (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277: 1-10.
12. Decognet, V., Bardin, M., Trottin-Caudal, Y., and Nicot, P.C. (2009) Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99: 185-193.
13. Desprez-Loustau, M.L., Vitasse, Y., Delzon, S., Capdevielle, X., Marcais, B., and Kremer, A. (2010) Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient. J Evol Biol 23: 87-97.
14. Dutech, C., Fabreguettes, O., Capdevielle, X., and Robin, C. (2010) Multiple introductions of divergent genetic lineages in an invasive fungal pathogen, Cryphonectria parasitica, in France. Heredity 105: 220-228.
15. Dutech, C., Barres, B., Bridier, J., Robin, C., Milgroom, M.G., and Ravigne, V. (2012) The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol Ecol 21: 3931-3946.
16. Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. (2004) Botrytis spp. and diseases they cause in agricultural systems - an introduction. In Botrytis: Biology, Pathology and Control. Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. (eds). Dordrecht: the Netherlands: Kluwer Academic Publishers, pp. 1-18.
17. Elmer, P.A.G., and Michailides, T.J. (2004) Epidemiology in Botrytis cinerea in orchard and vine crops. In Botrytis: Biology, Pathology and Control. Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. (eds). Dordrecht, the Netherlands: Kluwer Academic Publishers, pp. 243-262.
18. Evanno, G., Regnaut, S., and Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
19. Excoffier, L., and Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564-567.
20. Fournier, E., and Giraud, T. (2008) Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. J Evol Biol 21: 122-132.
21. Fournier, E., Giraud, T., Loiseau, A., Vautrin, D., Estoup, A., Solignac, M., etal. (2002) Characterization of nine polymorphic microsatellite loci in the fungus Botrytis cinerea (Ascomycota). Mol Ecol Notes 2: 253-255.
22. Fournier, E., Levis, C., Fortini, D., Leroux, P., Giraud, T., and Brygoo, Y. (2003) Characterization of Bc-hch, the Botrytis cinerea homolog of the Neurospora crassa het-c vegetative incompatibility locus, and its use as a population marker. Mycologia 95: 251-261.
23. Fournier, E., Giraud, T., Albertini, C., and Brygoo, Y. (2005) Partition of the Botrytis cinerea complex in France using multiple gene genealogies. Mycologia 97: 1251-1267.
24. Frenkel, O., Peever, T.L., Chilvers, M.I., Özkilinc, H., Can, C., Abbo, S., etal. (2010) Ecological genetic divergence of the fungal pathogen Didymella rabiei on sympatric wild and domesticated Cicer spp. (Chickpea). Appl Environ Microbiol 76: 30-39.
25. Giraud, T., Fortini, D., Levis, C., Leroux, P., and Brygoo, Y. (1997) RFLP markers show genetic recombination in Botryotinia fuckeliana (Botrytis cinerea) and transposable elements reveal two sympatric species. Mol Biol Evol 14: 1177-1185.
26. Giraud, T., Villareal, L., Austerlitz, F., Le Gac, M., and Lavigne, C. (2006) Importance of the life cycle in sympatric host race formation and speciation of pathogens. Phytopathology 96: 280-287.
27. Giraud, T., Gladieux, P., and Gavrilets, S. (2010) Linking the emergence of fungal plant diseases with ecological speciation. Trends Eco Evol 25: 387-395.
28. Gladieux, P., Zhang, X.G., Afoufa-Bastien, D., Sanhueza, R.M.V., Sbaghi, M., and Le Cam, B. (2008) On the origin and spread of the scab disease of apple: out of central Asia. PLoS ONE 3: e1455. doi:10.1371/journal.pone .0001455
29. Gladieux, P., Zhang, X.G., Roldan-Ruiz, I., Caffier, V., Leroy, T., Devaux, M., etal. (2010) Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol Ecol 19: 658-674.
30. Gladieux, P., Vercken, E., Fontaine, M.C., Hood, M.E., Jonot, O., Couloux, A., and Giraud, T. (2011a) Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28: 459-471.
31. Gladieux, P., Guerin, F., Giraud, T., Caffier, V., Lemaire, C., Parisi, L., etal. (2011b) Emergence of novel fungal pathogens by ecological speciation: importance of the reduced viability of immigrants. Mol Ecol 20: 4521-4532.
32. Gordon, T.R., and Leveau, J.H.J. (2010) Plant pathology: a story about biology. Annu Rev Phytopathol, 48: 293-309.
33. Isenegger, D.A., Ades, P.K., Ford, R., and Taylor, P.W.J. (2008) Status of the Botrytis cinerea species complex and microsatellite analysis of transposon types in South Asia and Australia. Fungal Divers 29: 17-26.
34. Jakobsson, M., and Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801-1806.
35. Jaspers, M.V., Seyb, A.M., Trought, M.C.T., and Balasubramaniam, R. (2013) Overwintering grapevine debris as an important source of Botrytis cinerea inoculum. Plant Pathol 62: 130-138.
36. Johnston, P.R., Hoksbergen, K., Park, D., and Beever, R.E. (2014) Genetic diversity of Botrytis in New Zealand vineyards and the significance of its seasonal and regional variation. Plant Pathol 63: 888-898.
37. Jombart, T. (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405.
38. Jombart, T., Devillard, S., and Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94.
39. Karchani-Balma, S., Gautier, A., Raies, A., and Fournier, E. (2008) Geography, plants and growing systems shape the genetic structure of Tunisian Botrytis cinerea populations. Phytopathology 98: 1271-1279.
40. Leroux, P., Gredt, M., Leroch, M., and Walker, A.-S. (2010) Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Appl Environ Microbiol 76: 6615-6630.
41. Ma, Z.H., and Michailides, T.J. (2005) Genetic structure of Botrytis cinerea populations from different host plants in California. Plant Dis 89: 1083-1089.
42. McDonald, B.A., and Linde, C. (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124: 163-180.
43. Martinez, F., Dubos, B., and Fermaud, M. (2005) The role of saprotrophy and virulence in the population dynamics of Botrytis cinerea in vineyards. Phytopathology 95: 692-700.
44. Martinez, F., Corio-Costet, M.F., Levis, C., Coarer, M., and Fermaud, M. (2008) New PCR primers applied to characterize distribution of Botrytis cinerea populations in French vineyards. Vitis 47: 217-226.
45. Mboup, M., Bahri, B., Leconte, M., De Vallavieille-Pope, C., Kaltz, O., and Enjalbert, J. (2012) Genetic structure and local adaptation of European wheat yellow rust populations: the role of temperature-specific adaptation. Evol Appl 5: 341-352.
46. Milgroom, M.G., and Peever, T.L. (2003) Population biology of plant pathogens - the synthesis of plant disease epidemiology and population genetics. Plant Dis 87: 608-617.
47. Morgan, J.A.T., Vredenburg, V.T., Rachowicz, L.J., Knapp, R.A., Stice, M.J., Tunstall, T., etal. (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. PNAS 104: 13845-13850.
48. Munkacsi, A.B., Stoxen, S., and May, G. (2008) Ustilago maydis populations tracked maize through domestication and cultivation in the Americas. Proc R Soc B Biol Sci 275: 1037-1046.
49. Munoz, G., Hinrichsen, P., Brygoo, Y., and Giraud, T. (2002) Genetic characterisation of Botrytis cinerea populations in Chile. Mycol Res 106: 594-601.
50. Peever, T.L., Olsen, L., Ibanez, A., and Timmer, L.W. (2000) Genetic differentiation and host specificity among populations of Alternaria spp. causing brown spot of grapefruit and tangerine x grapefruit hybrids in Florida. Phytopathology 90: 407-414.
51. Pritchard, J.K., Stephens, M., and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
52. Rajaguru, B.A.P., and Shaw, M.W. (2010) Genetic differentiation between hosts and locations in populations of latent Botrytis cinerea in southern England. Plant Pathol 59: 1081-1090.
53. Raymond, M., and Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Heredity 86: 248-249.
54. Robert, S., Ravigne, V., Zapater, M.F., Abadie, C., and Carlier, J. (2012) Contrasting introduction scenarios among continents in the worldwide invasion of the banana fungal pathogen Mycosphaerella fijiensis. Mol Ecol 21: 1098-1114.
55. Roca, M.G., Weichert, M., Siegmund, U., Tudzynski, P., and Fleissner, A. (2012) Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116: 379-387.
56. Samuel, S., Veloukas, T., Papavasileiou, A., and Karaoglanidis, G.S. (2012) Differences in frequency of transposable elements presence in Botrytis cinerea populations from several hosts in Greece. Plant Dis 96: 1286-1290.
57. Simwami, S.P., Khayhan, K., Henk, D.A., Aanensen, D.M., Boekhout, T., Hagen, F., etal. (2011) Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog 7: e1001343. doi:10.1371/journal.ppat.1001343.
58. Stukenbrock, E.H., and McDonald, B.A. (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46: 75-100.
59. Taylor, J.W., and Fisher, M.C. (2003) Fungal multilocus sequence typing - it's not just for bacteria. Curr Opin Microbiol 6: 351-356.
60. Taylor, J.W., Turner, E., Townsend, J.P., Dettman, J.R., and Jacobson, D. (2006) Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philos Trans R Soc B Biol Sci 361: 1947-1963.
61. The Angiosperm Phylogeny Group. (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161: 105-121.
62. Walker, A.-S., Gautier, A., Confais, J., Martinho, D., Viaud, M., Le Pecheur, P., etal. (2011) Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101: 1433-1445.
63. Weir, B.S., and Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38: 1358-1370.
64. Williams, P.D. (2010) Darwinian interventions: taming pathogens through evolutionary ecology. Trends Parasitol 26: 83-92.
65. Williamson, B., Tudzynsk, B., Tudzynski, P., and van Kan, J.A.L. (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8: 561-580.
66. Zhan, J.S., and McDonald, B.A. (2011) Thermal adaptation in the fungal pathogen Mycosphaerella graminicola. Mol Ecol 20: 1689-1701.