Fitness costs associated with unnecessary virulence factors and life history traits: Evolutionary insights from the potato late blight pathogen Phytophthora infestans

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Montarry, Josselin ^a,b   Hamelin, Frédéric M ^a   Glais, Isabelle ^a   Corbi, Roselyneère ^a   Andrivon, Didier ^a  

^a AGROCAMPUS OUEST   (France)

^b INRA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; CULTIVAR; FITNESS; FUNGUS; GENE EXPRESSION; HOST-PATHOGEN INTERACTION; LIFE HISTORY TRAIT; PATHOGENICITY; POTATO; SPORULATION; TRADE-OFF; VIRULENCE;

BACTERIA (MICROORGANISMS); PHYTOPHTHORA INFESTANS; SOLANUM TUBEROSUM;

VIRULENCE FACTOR;

ARTICLE; EVOLUTION; GENETICS; GENOTYPE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PHYTOPHTHORA INFESTANS; PLANT DISEASE; POTATO; VIRULENCE;

BIOLOGICAL EVOLUTION; GENOTYPE; PHYTOPHTHORA INFESTANS; PLANT DISEASES; SOLANUM TUBEROSUM; VIRULENCE; VIRULENCE FACTORS;

EID: 77956596099     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-283     Document Type: Article

References (61)

1. The complementary genic systems in flax and flax rust. HH Flor, Adv Genet 1956 8 29 54 full-text
2. Current status of gene-for-gene concept. HH Flor, Annu Rev Phytopathol 1971 9 275 296 10.1146/annurev.py.09.090171.001423
3. JE Vanderplank, Plant Diseases: Epidemics and Control New York: Academic Press 1963
4. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. KF Pedley GB Martin, Annu Rev Phytopathol 2003 41 215 243 10.1146/annurev.phyto.41.121602.143032 14527329
5. Can the strategic use of disease resistant hosts protect their inherent durability? MS Wolfe, Durability of Disease Resistance Dordrecht: Kluwer Academic Publishers, Jacobs T, Parlevliet JE, 1993 83 96
6. Classical plant breeding for durable resistance to diseases. R Johnson, J Plant Pathol 2000 82 3 7
7. Can the durability of resistance be predicted? LA Boyd, J Sci Food Agr 2006 86 2523 2526 10.1002/jsfa.2648
8. JF Crow, Basic concepts in population, quantitative, and evolutionary genetics New York: Academic Press 1986
9. Aggressiveness and its role in the adaptation of fungal plant pathogens. B Pariaud V Ravigné F Halkett H Goyeau J Carlier C Lannou, Plant Pathol 2009 58 409 424 10.1111/j.1365-3059.2009.02039.x
10. JE Vanderplank, Disease Resistance in Plants New York: Academic Press 1968
11. Stability of genetic polymorphism in host-parasite interactions. A Tellier JKM Brown, Proc Royal Soc London B- Biol Sci 2007 274 809 817 10.1098/rspb.2006.0281
12. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. CM Vera-Cruz J Bai I Ona H Leung RJ Nelson TW Mew JE Leach, Proc Natl Acad Sci USA 2000 97 13500 13505 10.1073/pnas.250271997 11095723
13. Prospects for understanding avirulence gene function. FF White B Yang LB Johnson, Curr Opin Plant Biol 2000 3 291 298 10.1016/S1369-5266(00)00082-0 10873850
14. Avirulence proteins of plant pathogens: determinants of victory and defeat. R Luderer MHAJ Joosten, Mol Plant Pathol 2001 2 355 364 10.1046/j.1464-6722.2001.00086.x 20573025
15. Microbial avirulence determinants: guided missiles or antigenic flak? P Skamnioti CJ Ridout, Mol Plant Pathol 2005 6 551 559 10.1111/j.1364-3703.2005. 00302.x 20565679
16. Pathogen fitness penalty as a predictor of durability of disease resistance genes. JE Leach CMV Cruz JF Bai H Leung, Annu Rev Phytopathol 2001 39 187 224 10.1146/annurev.phyto.39.1.187 11701864
17. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. J Bai SH Choi G Ponciano H Leung JE Leach, Mol Plant-Microbe Interact 2000 13 1322 1329 10.1094/MPMI.2000.13.12.1322 11106024
18. A fitness cost for Turnip mosaic virus to overcome host resistance. CE Jenner X Wang F Ponz JA Walsh, Virus Res 2002 86 1 6 10.1016/S0168-1702(02) 00031-X 12076824
19. Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). YJ Huang ZQ Li N Evans T Rouxel BDL Fitt MH Balesdent, Eur J Plant Pathol 2006 114 77 89 10.1007/s10658-005-2643-4
20. Evolution of virulence in a plant host-pathogen metapopulation. PH Thrall JJ Burdon, Science 2003 299 1735 1737 10.1126/science.1080070 12637745
21. Population structure of plant pathogenic fungi and bacteria. H Leung RJ Nelson JE Leach, Advances in Plant Pathology New York: Academic Press, Andrews JH, Tommenup IC, 1993 10 157 205
22. Genetic variation in pathogen populations and its implications for adaptation to host resistance. JJ Burdon, Durability of Disease Resistance Dordrecht: Kluwer Academic Publishers, Jacobs T, Parlevliet JE, 1993 41 56
23. Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f. sp. tritici. B Bahri O Kaltz M Leconte C de Vallavieille-Pope J Enjalbert, BMC Evol Biol 2009 9 26 10.1186/1471-2148-9-26 19183485
24. Adaptation of Phytophthora infestans to partial resistance in potato: Evidence from French and Moroccan populations. D Andrivon F Pilet J Montarry M Hafidi R Corbière EH Achbani R Pellé D Ellissèche, Phytopathology 2007 97 338 343 10.1094/PHYTO-97-3-0338 18943654
25. Adaptation to the most abundant host genotype in an agricultural plant-pathogen system - potato late blight. J Montarry I Glais R Corbiere D Andrivon, J Evol Biol 2008 21 1397 1407 10.1111/j.1420-9101.2008.01557.x 18547352
26. GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. S Arnaud-Haond K Belkhir, Mol Ecol Notes 2007 7 15 17 10.1111/j.1471-8286.2006.01522.x
27. Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans. J Montarry D Andrivon I Glais R Corbière G Mialdea F Delmotte, Mol Ecol 2010 19 1965 1977 10.1111/j.1365-294X.2010.04619.x 20345671
28. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. BJ Haas S Kamoun MC Zody RHY Jiang RE Handsaker LM Cano M Grabherr CD Kodira S Raffaele T Torto-Alalibo, et al. Nature 2009 461 393 398 10.1038/nature08358 19741609
29. Races of Phytophthora infestans in France, 1991-1993. D Andrivon, Potato Res 1994 37 279 286 10.1007/BF02360520
30. Evolution of Phytophthora infestans populations in the two most important potato production areas in France during 1992-1996. L Lebreton C Laurent D Andrivon, Plant Pathol 1998 47 427 439 10.1046/j.1365-3059.1998.00265.x
31. Host adaptation in Phytophthora infestans: a review from a population biology perspective. D Andrivon R Corbière L Lebreton F Pilet J Montarry R Pellé D Ellissèche, Plant Breed Seed Sci 2004 50 15 27
32. Race structure and dynamics in populations of Phytophthora infestans. D Andrivon, Can J Bot 1994 72 1681 1687 10.1139/b94-206
33. Persistence of complex virulences in populations of Phytophthora infestans in Western Washington. ML Derie DA Inglis, Phytopathology 2001 91 606 612 10.1094/PHYTO.2001.91.6.606 18943951
34. Race diversity and complexity in selected populations of fungal biotrophic pathogens of cereals. D Andrivon C de Vallavieille-Pope, Phytopathology 1995 85 897 905 10.1094/Phyto-85-897
35. Reducing the cost of resistance; experimental evolution in the filamentous fungus Aspergillus nidulans. SE Schoustra AJM Debets M Slakhorst RF Hoekstra, J Evol Biol 2006 19 1115 1127 10.1111/j.1420-9101.2006.01102.x 16780512
36. A systematic study of the genetic response of a variable virus to the introduction of deleterious mutations in a functional capsid region. E Luna A Rodriguez-Huete V Rincon R Mateo MG Mateu, J Virol 2009 83 10140 10151 10.1128/JVI.00903-09 19625409
37. Periodic host absence can select for higher or lower parasite transmission rates. F van den Berg N Bacaer JAJ Metz C Lannou F van den Bosch, Evol Ecol 2010
38. Recent and future developments in potato fungal pathology. B Schöber LJ Turkensteen, Neth J Plant Pathol 1992 98 suppl 2 73 83 10.1007/BF01974474
39. Effector genes of Xanthamonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. G Wichmann J Bergelson, Genetics 2004 166 693 706 10.1534/genetics.166.2.693 15020460
40. Polymorphism in multilocus host-parasite coevolutionary interactions. A Tellier JKM Brown, Genetics 2007 177 1777 1790 10.1534/genetics.107.074393 17947440
41. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. A Palloix V Ayme B Moury, New Phytol 2009 183 190 199 10.1111/j.1469-8137.2009.02827.x 19344475
42. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. H Brun AM Chevre B Fitt S Powers AL Besnard M Ermel V Huteau B Marquer F Eber M Renard D Andrivon, New Phytol 2010 185 285 299 10.1111/j.1469-8137.2009.03049.x 19814776
43. How can we achieve durable disease resistance in agricultural ecosystems? B McDonald, New Phytol 2010 185 3 5 10.1111/j.1469-8137.2009.03108.x 20088970
44. Pyramiding major genes for resistance to maintain residual effects. WL Pedersen S Leath, Annu Rev Phytopathol 1988 26 369 378 10.1146/annurev.py.26. 090188.002101
45. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. LPNM Kroon FT Bakker GBM van den Bosch PJM Bonants WG Flier, Fungal Genet Biol 2004 41 766 782 10.1016/j.fgb.2004.03.007 15219561
46. Phytophthora infestans. CJ Alexopoulos CW Mims M Blackwell, Introductory Mycology John Wiley and Sons 4 1994 717 720
47. Effects of the aerial environment on late blight of potato foliage - a review. JG Harrison, Plant Pathol 1992 41 384 416 10.1111/j.1365-3059.1992. tb02435.x
48. Emergence of potato blight, 1843-46. PMA Bourke, Nature 1964 203 805 808 10.1038/203805a0
49. Production and germination of oospores of Phytophthora infestans. JJ Smoot FJ Gough HA Lamey JJ Eichenmuller ME Gallegly, Phytopathology 1958 48 165 171
50. Development of potato late blight epidemics: disease foci, disease gradients and infection sources. MJ Zwankhuizen F Govers JC Zadoks, Phytopathology 1998 88 754 763 10.1094/PHYTO.1998.88.8.754 18944880
51. Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland. G Knapova U Gisi, Plant Pathol 2002 51 641 653 10.1046/j.1365-3059.2002.00750.x
52. Novel microsatellite markers for the analysis of Phytophthora infestans populations. AK Lees R Wattier DS Shaw L Sullivan NA Williams DEL Cooke, Plant Pathol 2006 55 311 319 10.1111/j.1365-3059.2006.01359.x
53. The R3 resistance to Phytophthora infestans in potato is conferred by two closely linked R genes with distinct specificities. SW Huang V Vleeshouvers JS Werij RCB Hutten HJ van Eck RGF Visser E Jacobsen, Mol Plant-Microbe Interact 2004 17 428 435 10.1094/MPMI.2004.17.4.428 15077675
54. Effect of plant age and inoculum concentration on expression of major gene resistance to Phytophthora infestans in detached potato leaflets. HE Stewart, Mycol Res 1990 94 823 826 10.1016/S0953-7562(09)81385-3
55. Virulence of Phytophthora infestans: its stability and variability assessed in a ring test across European laboratories. D Andrivon J Avendão-Cárcoles AM Cameron SF Carnegie LR Cooke R Corbière D Detourné LJ Dowley D Evans K Forisekova DG Griffin A Hannukkala AK Lees R Lebecka F Niepold Z Polgar DS Shaw J Thompson B Trognitz HMG van Raaij E Zimnoch-Guzowska, Plant Pathol
56. A G-alpha subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans. M Latijnhouwers W Ligterink VGAA Vleeshouwers P Van West F Govers, Mol Microbiol 2004 51 925 936 10.1046/j.1365-2958.2003.03893.x 14763970
57. Compartmental models in epidemiology. F Brauer, Matematical epidemiology. Lecture Notes in Matematics Springer series, Brauer et al., 2008 1945 19 79
58. LV Madden G Hughes F van den Bosch, The study of plant disease epidemics St Paul, MN: APS Press 2007
59. Further notes on the basic reproduction number. P van den Driessche J Watmough, Matematical epidemiology. Lecture Notes in Matematics Springer series, Brauer et al., 2008 1945 81 130
60. A beginners guide to adaptive dynamics. OA Diekmann, Mathematical modeling of population dynamics Warszawa: Banach Center Publications, Institute of Mathematics, Polish Academy of Sciences 2004 63 47 86
61. Model selection in ecology and evolution. JB Johnson KS Omland, Trends Ecol Evol 2004 19 101 108 10.1016/j.tree.2003.10.013 16701236