Differential selection pressures exerted by host resistance quantitative trait loci on a pathogen population: A case study in an apple × Venturia inaequalis pathosystem

New Phytologist

Volumn 197, Issue 3, 2013, Pages 899-908

  Van, Amandine Lê ^a,b   Caffier, Valérie ^a,b   Lasserre Zuber, Pauline ^a,b   Chauveau, Aurélie ^c   Brunel, Dominique ^c   Le Cam, Bruno ^a,b   Durel, Charles Eric ^a,b  

^a Universite d'Angers   (France)

^b UNIVERSITÉ D'ANGERS   (France)

^c CENTRE NATIONAL DE GÉNOTYPAGE   (France)

Author keywords

Broad spectrum resistance; Durability; Malus domestica; Quantitative pyrosequencing; Quantitative resistance; Resistance erosion; Selection pressure; Venturia inaequalis

Indexed keywords

AGRICULTURAL MANAGEMENT; COEVOLUTION; CULTIVAR; DECIDUOUS TREE; DISEASE CONTROL; DISEASE RESISTANCE; FUNGUS; GENETIC ANALYSIS; GENOTYPE; HOST PLANT; NATURAL SELECTION; PATHOGEN;

LONCHOCARPUS CAPASSA; MALUS; MALUS X DOMESTICA; VENTURIA INAEQUALIS;

EID: 84872127481     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12086     Document Type: Article

References (56)

1. Abang MM, Baum M, Ceccarelli S, Grando S, Linde CC, Yahyaoui A, Zhan JS, McDonald BA. 2006. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96: 1214-1222.
2. Aldrich J, Cullis CA. 1993. CTAB DNA extraction from plant tissues. Plant Molecular Biology Reporter 11: 128-141.
3. Andrivon D, Pilet F, Montarry J, Hafidi M, Corbiere R, Achbani EH, Pelle R, Ellisseche D. 2007. Adaptation of Phytophthora infestans to partial resistance in potato: evidence from French and Moroccan populations. Phytopathology 97: 338-343.
4. Antonovics J, Thrall PH, Burdon JJ, Laine AL. 2011. Partial resistance in the Linum-Melampsora host-pathogen system: does partial resistance make the red queen run slower? Evolution 65: 512-522.
5. Barrett LG, Thrall PH, Burdon JJ, Linde CC. 2008. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution 23: 678-685.
6. Bayles RA, Flath K, Hovmoller MS. 2000. Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe. Agronomie 20: 805-811.
7. Benson AK, Kelly SA, Legge R, Ma FR, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua KJ et al. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences, USA 107: 18933-18938.
8. Brun H, Chèvre A-M, Fitt BD, Powers S, Besnard A-L, Ermel M, Huteau V, Marquer B, Eber F, Renard M et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytologist 185: 285-299.
9. Caffier V, Laurens F. 2005. Breakdown of Pl2, a major gene of resistance to apple powdery mildew, in a French experimental orchard. Plant Pathology 54: 116-124.
10. Calenge F, 2004. Organisation génomique globale des facteurs de résistance à la tavelure (Venturia inaequalis), à l'oïdium (Podosphaera leucotricha) et au feu bactérien (Erwinia amylovora) chez le pommier (Malus × domestica Borkh.). PhD thesis, University of Angers, Angers, France.
11. Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg WE, Parisi L, Durel CE. 2004. Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94: 370-379.
12. Charcosset A, Mangin B, Moreau L, Combes L, Jourjon MF, Gallais A. 2000. Heterosis in maize investigated using connected RIL populations. In: Gallais A, Dillmann C, Goldringer I, eds. Quantitative genetics and breeding methods: the way ahead. Paris, France: Les colloques de l'INRA no. 96, 89-98.
13. Christiansen MJ, Feenstra B, Skovgaard IM, Andersen SB. 2006. Genetic analysis of resistance to yellow rust in hexaploid wheat using a mixture model for multiple crosses. Theoretical and Applied Genetics 112: 581-591.
14. Churchill GA, Doerge RW. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
15. Fabre F, Rousseau E, Mailleret L, Moury B. 2012. Durable strategies to deploy plant resistance in agricultural landscapes. New Phytologist 193: 1064-1075.
16. Gandon S, Michalakis Y. 2002. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15: 451-462.
17. Gladieux P, Guerin F, Giraud T, Caffier V, Lemaire C, Parisi L, Didelot F, Le Cam B. 2011. Emergence of novel fungal pathogens by ecological speciation: importance of the reduced viability of immigrants. Molecular Ecology 20: 4521-4532.
18. Gladieux P, Zhang XG, Afoufa-Bastien D, Sanhueza RMV, Sbaghi M, Le Cam B. 2008. On the origin and spread of the scab disease of apple: out of Central Asia. PLoS ONE 3: e1455.
19. Gladieux P, Zhang XG, Róldan-Ruiz I, Caffier V, Leroy T, Devaux M, Van Glabeke S, Coart E, Le Cam B. 2010. Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Molecular Ecology 19: 658-674.
20. Guerin F, Le Cam B. 2004. Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalis. Phytopathology 94: 364-369.
21. Johnson R. 1981. Durable resistance - definition of, genetic control, and attainment in plant breeding. Phytopathology 71: 567-568.
22. Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C. 2005. Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytologist 167: 113-127.
23. Jourjon MF, Jasson S, Marcel J, Ngom B, Mangin B. 2005. MCQTL: multi-allelic QTL mapping in multi-cross design. Bioinformatics 21: 128-130.
24. Kou YJ, Wang SP. 2010. Broad-spectrum and durability: understanding of quantitative disease resistance. Current Opinion in Plant Biology 13: 181-185.
25. Kucheryava N, Bowen JK, Sutherland PW, Conolly JJ, Mesarich CH, Rikkerink EHA, Kemen E, Plummer KM, Hahn M, Templeton MD. 2008. Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane. Fungal Genetics and Biology 45: 1329-1339.
26. Lannou C. 2001. Intrapathotype diversity for aggressiveness and pathogen evolution in cultivar mixtures. Phytopathology 91: 500-510.
27. Laurens F, Chevalier M, Dolega E, Gennari F, Goerre M, Fischer C, Kellerhals M, Lateur M, Lefrancq B, Parisi L et al. 2004. Local European cultivars as sources of durable scab resistance in apple. Acta Horticulturae 663: 115-121.
28. Le Guen V, Garcia D, Mattos CRR, Doare F, Lespinasse D, Seguin M. 2007. Bypassing of a polygenic Microcyclus ulei resistance in rubber tree, analyzed by QTL detection. New Phytologist 173: 335-345.
29. Lê Van A, Gladieux P, Lemaire C, Cornille A, Giraud T, Durel C-E, Caffier V, Le Cam B. 2012. Evolution of pathogenicity traits in the apple scab fungal pathogen in response to the domestication of its host. Evolutionary Applications 5: 694-704.
30. Lehman JS, Shaner G. 2007. Heritability of latent period estimated from wild-type and selected populations of Puccinia triticina. Phytopathology 97: 1022-1029.
31. Lindhout P. 2002. The perspectives of polygenic resistance in breeding for durable disease resistance. Euphytica 124: 217-226.
32. Marcel TC, Gorguet B, Truong TAM, Kohutova Z, Vels A, Niks RE. 2008. Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytologist 177: 743-755.
33. McDonald BA, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40: 349-379.
34. Miedaner T, Schilling AG, Geiger HH. 2004. Competition effects among isolates of Fusarium culmorum differing in aggressiveness and mycotoxin production on heads of winter rye. European Journal of Plant Pathology 110: 63-70.
35. Montarry J, Corbiere R, Lesueur S, Glais I, Andrivon D. 2006. Does selection by resistant hosts trigger local adaptation in plant-pathogen systems? Journal of Evolutionary Biology 19: 522-531.
36. Palloix A, Ayme V, Moury B. 2009. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytologist 183: 190-199.
37. Palumbi SR. 2001. Humans as the world's greatest evolutionary force. Science 293: 1786-1790.
38. Parisi L, Lespinasse Y, Guillaumes J, Krüger J. 1993. A new race of Venturia inaequalis virulent to apples with resistance due to the Vf gene. Phytopathology 83: 533-537.
39. Parlevliet JE. 2002. Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124: 147-156.
40. Parlevliet JE, Zadoks JC. 1977. The integrated concept of disease resistance: a new view including horizontal and vertical resistance in plants. Euphytica 26: 5-21.
41. Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G, Testolin R, Merdinoglu D, Mestre P. 2010. Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biology 10: 147.
42. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 2009. Shades of gray: the world of quantitative disease resistance. Trends in Plant Science 14: 21-29.
43. R-Development-Core-team. 2008. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.
44. Regoes RR, Nowak MA, Bonhoeffer S. 2000. Evolution of virulence in a heterogeneous host population. Evolution 54: 64-71.
45. Rouxel T, Penaud A, Pinochet X, Brun H, Gout L, Delourme R, Schmit J, Balesdent MH. 2003. A 10-year survey of population of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. European Journal of Plant Pathology 109: 871-881.
46. Sapoukhina N, Durel CE, Le Cam B. 2009. Spatial deployment of gene-for-gene resistance governs evolution and spread of pathogen populations. Theoretical Ecology 2: 229-238.
47. Sommerhalder RJ, McDonald BA, Mascher F, Zhan J. 2011. Effect of hosts on competition among clones and evidence of differential selection between pathogenic and saprophytic phases in experimental populations of the wheat pathogen Phaeosphaeria nodorum. BMC Evolutionary Biology 11: 188.
48. Soufflet-Freslon V, Gianfranceschi L, Patocchi A, Durel CE. 2008. Inheritance studies of apple scab resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum QTL. Genome 51: 657-667.
49. Stokstad E. 2007. Deadly wheat fungus threatens world's breadbaskets. Science 315: 1786-1787.
50. Talukder ZI, Tharreau D, Price AH. 2004. Quantitative trait loci analysis suggests that partial resistance to rice blast is mostly determined by race-specific interactions. New Phytologist 162: 197-209.
51. Thompson JN, Burdon JJ. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360: 121-125.
52. Thrall PH, Burdon JJ. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299: 1735-1737.
53. ® 5, software for the mapping of quantitative trait loci in experimental populations. Wageningen, the Netherlands: Kyazma BV.
54. Vergne E, Grand X, Ballini E, Chalvon V, Saindrenan P, Tharreau D, Notteghem JL, Morel JB. 2010. Preformed expression of defense is a hallmark of partial resistance to rice blast fungal pathogen Magnaporthe oryzae. BMC Plant Biology 10: 17.
55. Von der Ohe C, Miedaner T. 2011. Competitive aggressiveness in binary mixtures of Fusarium graminearum and F. culmorum isolates inoculated on spring wheat with highly effective resistance QTL. Journal of Phytopathology 159: 401-410.
56. Zhan J, Mundt CC, Hoffer ME, McDonald BA. 2002. Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. Journal of Evolutionary Biology 15: 634-647.