Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen f.sp.

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Analyses of large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. Analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen.

Vyšlo v časopise: Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen f.sp.. PLoS Pathog 10(1): e32767. doi:10.1371/journal.ppat.1003903
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003903

Souhrn

Zdroje

1. StukenbrockEH, McDonaldBA (2008) The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology 46: 75–100.

2. ParkerIM, GilbertGS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annual Review of Ecology, Evolution, and Systematics 35: 675–700.

3. PalmM (2001) Systematics and the impact of invasive fungi on agriculture in the United States. BioScience 51: 141–147.

4. SinghRP, HodsonDP, JinY, Huerta-EspinoJ, KinyuaMG, et al. (2006) Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Reviews 1: 054.

5. Singh RP, William HM, Huerta-Espino J, Rosewarne G (2004) Wheat rust in Asia: meeting the challenges with old and new technologies. In proceedings of the 4th International Crop Science Congress; 26 Sep–1 Oct 2004; Brisbane, Australia. Available at: http://www.cropscience.org.au/icsc2004/symposia/3/7/141_singhrp.htm.

6. HovmøllerMS, YahyaouiAH, MilusEA, JustesenAF (2008) Rapid global spread of two aggressive strains of a wheat rust fungus. Molecular Ecology 17: 3818–3826.

7. PerringsC, WilliamsonM, BarbierE, DelfinoD, DalmazzoneS, et al. (2002) Biological invasion risks and the public good: an economic perspective. Conservation Ecology 6: Article 1.

8. CampbellF (2001) The science of risk assessment for phytosanitary regulation and the impact of changing trade regulations. BioScience 51: 148–153.

9. BrownJKM, HovmøllerMS (2002) Aerial dispersal of fungi on the global and continental scales and its consequences for plant disease. Science 297: 537–541.

10. de Vallavieille-PopeC, AliS, LeconteM, EnjalbertJ, DelosM, et al. (2012) Virulence dynamics and regional structuring of Puccinia striiformis f. sp. tritici in France between 1984 and 2009. Plant Disease 96: 131–140.

11. HovmøllerMS, SørensenCK, WalterS, JustesenAF (2011) Diversity of Puccinia striiformis on cereals and grasses. Annual Review of Phytopathology 49: 197–217.

12. HovmøllerMS, WalterS, JustesenAF (2010) Escalating threat of wheat rusts. Science 329: 369.

13. AliS, ShahSJA, RahmanH, SaqibMS, IbrahimM, et al. (2009) Variability in wheat yield under yellow rust pressure in Pakistan. Turkish Journal of Agriculture and Forestry 33: 537–546.

14. AliS, ShahSJA, KhalilIH, RahmanH, MaqboolK, et al. (2009) Partial resistance to yellow rust in introduced winter wheat germplasm at the north of Pakistan. Australian Journal of Crop Science 3: 37–43.

15. WellingsCR (2007) Puccinia striiformis in Australia: A review of the incursion, evolution and adaptation of stripe rust in the period 1979–2006. Australian Journal of Agricultural Research 58: 567–575.

16. Stubbs RW (1985) Stripe rust. In: Roelfs AP, Bushnell WR, editors. The Cereal Rusts, Diseases, Distribution, Epidemiology and Control. London, UK: Academic Press. pp. 61–101.

17. Stubbs RW (1988) Pathogenicity analysis of yellow (stripe) rust of wheat and its significance in a global context. In: Simmonds NW, Rajaram S, editors. Breeding strategies for resistance to the rusts of wheat: CIMMYT D.F. Mexico.

18. KolmerJA (2005) Tracking wheat rust on a continental scale. Current Opinion in Plant Biology 8: 441–449.

19. JustesenAF, RidoutbCJ, HovmøllerMS (2002) The recent history of Puccinia striiformis f.sp. tritici in Denmark as revealed by disease incidence and AFLP markers. Plant Pathology 51: 13–23.

20. BoshoffWHP, PretoriusZA, van NiekerkBD (2002) Establishment, distribution, and pathogenicity of Puccinia striiformis f.sp. tritici in South Africa. Plant Disease 86: 485–492.

21. RudorfW, JobM (1934) Untersuchungen bezüglich des Spezialisierung von Puccinia graminis tritici. Puccinia trilicina und Puccinia glumarum tritici, sowie über Resistenz und ihre Vererbung in verschiedenen Kreuzungen. Pflanzenzüchtung 19: 333–365.

22. ChenXM (2005) Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology 27: 314–337.

23. MarkellSG, MilusEA (2008) Emergence of a Novel Population of Puccinia striiformis f. sp. tritici in Eastern United States. Phytopathology 98: 632–639.

24. MilusEA, KristensenK, HovmøllerMS (2009) Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f.sp. tritici causing stripe rust of wheat. Phytopathology 99: 89–94.

25. EnjalbertJ, DuanX, LeconteM, HovmøllerMS, de Vallavieille-PopeC (2005) Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France. Molecular Ecology 14: 2065–2073.

26. HovmøllerMS, JustesenAF, BrownJKM (2002) Clonality and long-distance migration of Puccinia striiformis f.sp. tritici in north-west Europe. Plant Pathology 51: 24–32.

27. ChenX, LineRF, LeungH (1993) Relationship between virulence variation and DNA polymorphism in Puccinia striiformis. Phytopathology 83: 1489–1497.

28. MboupM, LeconteM, GautierA, WanAM, ChenW, et al. (2009) Evidence of genetic recombination in wheat yellow rust populations of a Chinese oversummering area. Fungal Genetics and Biology 46: 299–307.

29. BahriB, ShahSJA, HussainS, LeconteM, EnjalbertJ, et al. (2011) Genetic diversity of wheat yellow rust population in Pakistan and its relationship with host resistance. Plant Pathology 60: 649–660.

30. HovmøllerMS, JustesenAF (2007) Appearance of atypical Puccinia striiformis f. sp. tritici phenotypes in north-western Europe. Australian Journal of Agricultural Research 58: 518–524.

31. BahriB, LeconteM, OuffroukhA, de Vallavieille-PopeC, EnjalbertJ (2009) Geographic limits of a clonal population of wheat yellow rust in the Mediterranean region. Molecular Ecology 18: 4165–4179.

32. AliS, LeconteM, WalkerA-S, EnjalbertJ, de Vallavieille-PopeC (2010) Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp. tritici. Fungal Genetics and Biology 47: 828–838.

33. EnjalbertJ, DuanX, GiraudT, VautrinC, de Vallavieille-PopeC, et al. (2002) Isolation of twelve microsatellite loci, using an enrichment protocol, in the phytopathogenic fungus Puccinia striiformis f. sp. tritici. Molecular Ecology Notes 2: 563–565.

34. AliS, GautierA, LeconteM, EnjalbertJ, De Vallavieille-PopeC (2011) A rapid genotyping method for an obligate fungal pathogen, Puccinia striiformis f.sp. tritici, based on DNA extraction from infected leaf and Multiplex PCR genotyping. BMC Research Notes 4: 240.

35. DutechC, FabreguettesO, CapdevielleX, RobinC (2010) Multiple introductions of divergent genetic lineages in an invasive fungal pathogen, Cryphonectria parasitica, in France. Heredity 105: 220–228.

36. JombartT, DevillardS, BallouxF (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 95 http://www.biomedcentral.com/1471-2156/1411/1494.

37. PritchardJK, StephensM, DonnellyP (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

38. GaoH, WilliamsonS, BustamanteCD (2007) A markov chain monte carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176: 1635–1651.

39. JakobssonM, RosenbergNA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.

40. NeiM, TajimaF, TatenoY (1983) Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution 19: 153–170.

41. Langella O (2008) POPULATIONS 1.2.3, Logiciel de génétique des populations. In: Langella O, editor. Gif-sur-Yvette, France: Laboratoire Populations, Génétique et évolution, CNRS.

42. Belkhir KBP, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000: Université de Montpellier II, Montpellier (France) http://www.univ-montp2.fr/~genetix/genetix/genetix.htm.

43. Arnaud-HaondS, BelkhirK (2007) GenClone 1.0: A new program to analyse genetics data on clonal organisms. Molecular Ecology Notes 7: 15–17.

44. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices.2.9.3 ed: Available from http://www2.unil.ch/popgen/softwares/fstat.htm.

45. AgapowPM, BurtA (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes 1: 101–102.

46. SzpiechZA, JakobssonM, RosenbergNA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498–2504.

47. RaymondM, RoussetF (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.

48. Maynard-Smith J, Smith NH, O'rourke M, Spratt BG. How clonal are bacteria?; 1993. pp. 4384–4388.

49. DilmaghaniA, GladieuxP, GoutL, GiraudT, BrunnerPC, et al. (2012) Migration patterns and changes in population biology associated with the worldwide spread of the oilseed rape pathogen Leptosphaeria maculans. Molecular Ecology 21 doi: 10.1111/j.1365-294X.2012.05535.x

50. CornilleA, GladieuxP, SmuldersMJM, Roldan-RuizI, LaurensF, et al. (2012) New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties. PLoS Genetics 8: e1002703 doi:1002710.1001371/journal.pgen.1002703

51. CornuetJM, RavigneV, EstoupA (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11: 401.

52. CsilléryK, FrançoisO, BlumM (2012) abc: an R package for approximate Bayesian computation (ABC). Methods in Ecology and Evolution 3: 475–479.

53. NeiM (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

54. WeirBS, CockerhamCC (1984) Estimating F-statistics for the analysis of population structure. Evolution Psychiatrique 38: 1358–1370.

55. GoldsteinDB, RuizLA, Cavalli-SforzaLL, FeldmanMW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463–471.

56. FagundesNJR, RayN, BeaumontMA, NeuenschwanderS, SalzanoFM, et al. (2007) Statistical evaluation of alternative models of human evolution. Proceedings of the National Academy of Science of the United States of America 104: 17614–17619.

57. CornuetJM, SantosF, BeaumontMA, RobertCP, MarinJM, et al. (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24: 2713–2719.

58. BeaumontMA, ZhangW, BaldingDJ (2002) Approximate Bayesian computation in population genetics. Genetics 162: 2025–2035.

59. EvannoG, RegnautS, GoudetJ (2005) Detecting the number of clusters of individuals using the software STRUCTURE : a simulation study. Molecular Ecology 14: 2611–2620.

60. GladieuxP, ZhangX-G, Afoufa-BastienD, SanhuezaR-MV, SbaghiM, et al. (2008) On the origin and spread of the scab disease of apple: out of Central Asia. PLoS ONE 3: e1455.

61. SchoflG, SchlottererC (2006) Microsatellite variation and differentiation in African and non-African populations of Drosophila simulans. Molecular Ecology 15: 3895–3905.

62. Cummins GB (1971) The rusts fungi of cereals, grasses, and bamboos: Springer-Verlag, New York.

63. JinY, SzaboLJ, CarsonM (2010) Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an Alternate Host. Phytopathology 100: 432–435.

64. RayR, GururajaKV, RamchandraTV (2011) Predictive distribution modeling for rare Himalayan medicinal plant Berberis aristata DC. Journal of Environmental Biology 32: 725–730.

65. PerveenA, QaiserM (2010) Pollen flora of Pakistan–LXV. berberidaceae. Pakistan Journal of Botany 42: 1–6.

66. AliS, GladieuxP, RahmanH, SaqibMS, FiazM, et al. (2014) 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. Molecular Ecology DOI: 10.1111/mec.12629

67. CarletonMA (1915) A serious new wheat rust in this country. Science 42: 58–59.

68. MilusEA, SeyranE, McNewR (2006) Aggressiveness of Puccinia striiformis f. sp. tritici isolates in the South-Central United States. Plant Disease 90: 847–852.

69. WellingsCR, WrightDG, KeiperF, LoughmanR (2003) First detection of wheat stripe rust in Western Australia: evidence for a foreign incursion. Australasian Plant Pathology 32: 321–322.

70. GiraudT, GladieuxP, GavriletsS (2010) Linking the emergence of fungal plant diseases with ecological speciation. Trends in Ecology & Evolution 25: 387–395.

71. BultinR (2002) The costs and benefits of sex: new insights from old asexual lineages. Nature Reviews Genetics 3: 313–317.