Genetic differentiation at microsatellite loci among populations of Mycosphaerella graminicola from California, Indiana, Kansas, and North Dakota

Phytopathology

Volumn 101, Issue 10, 2011, Pages 1251-1259

  Gurung, Suraj ^a,e   Goodwin, Stephen B ^b   Kabbage, Mehdi ^c   Bockus, William W ^d   Adhikari, Tika B ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d KANSAS STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Genetic diversity

Indexed keywords

MICROSATELLITE DNA;

ARTICLE; ASCOMYCETES; FLOWER; FUNGAL GENE; GENETIC DRIFT; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; GENOTYPE; HAPLOTYPE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PLANT DISEASE; UNITED STATES; WHEAT;

ASCOMYCOTA; CALIFORNIA; GENES, MATING TYPE, FUNGAL; GENETIC DRIFT; GENETIC MARKERS; GENETIC VARIATION; GENOTYPE; GERM CELLS, PLANT; HAPLOTYPES; INDIANA; KANSAS; MICROSATELLITE REPEATS; NORTH DAKOTA; PLANT DISEASES; TRITICUM;

MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

EID: 80655131223     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-08-10-0212     Document Type: Article

References (52)

1. Abrinbana, M., Mozafiri, J., Shams-bakhsh, M., and Mehrabi, R. 2010. Genetic structure of Mycosphaerella graminicola populations in Iran. Plant Pathol. 59:829-838.
2. Adhikari, T. B., Ali, S., Burlakoti, R. R., Singh, P. K., Mergoum, M., and Goodwin, S. B. 2008. Genetic structure of Phaeosphaeria nodorum populations in the North-Central and Midwestern United States. Phytopathology 98:101-107.
3. Agapow, P. M., and Burt, A. 2001. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1:101-102. (Pubitemid 33691862)
4. Bearchell, S. J., Fraaije, B. A., Shaw, M. W., and Fitt, B. D. L. 2005. Wheat archive links long-term fungal pathogen population dynamics to air pollution. Proc. Natl. Acad. Sci. USA 102:5438-5442.
5. Boeger, J. M., Chen, R. S., and McDonald, B. A. 1993. Gene flow between geographic populations of Mycosphaerella graminicola (anamorph Septoria tritici) detected with restriction fragment length polymorphism markers. Phytopathology 83:1148-1154. (Pubitemid 2023119)
6. Brown, J. K. M., and Hovmøller, M. S. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537-541. (Pubitemid 34815327)
7. Chartouni, L. E., Tisserant, B., Siah, A., Duyme, F., Leducq, J. B., Deweer, C., Roisin, C. F., Sanssené, J., Durand, R., Halama, P., and Reignault, P. P. 2011. Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia. Online publication. doi:10.3852/10-184.
8. Chen, R. S., and McDonald, B. A. 1996. Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics 142:1119-1127. (Pubitemid 26115495)
9. Cowger, C., McDonald, B. A., and Mundt, C. C. 2002. Frequency of sexual reproduction by Mycosphaerella graminicola on partially resistant wheat cultivars. Phytopathology 92:1175-1181. (Pubitemid 35235597)
10. Eriksen, L., Shaw, M. W., and Østergård, H. 2001. A model of the effect of pseudothecia on genetic recombination and epidemic development in populations of Mycosphaerella graminicola. Phytopathology 91:240-248. (Pubitemid 32183977)
11. Everitt, B. S. 1977. The Analysis of Contingency Tables. Wiley, New York.
12. Excoffier, L., Laval, G., and Schneider, S. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinf. 1:47-50.
13. Excoffier, L., Smouse, P. E., and Quattro, J. M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479-491.
14. Eyal, Z. 1981. Integrated control of Septoria diseases of wheat. Plant Dis. 65:763-768.
15. Eyal, Z., Scharen, A. L., Huffman, M. D., and Prescott, J. M. 1985. Global insights into virulence frequencies of Mycosphaerella graminicola. Phytopathology 75:1456-1462.
16. Goodwin, S. B., Ben M'Barek, S., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., Foster, A. J., Van der Lee, T. A. J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., van der Burgt, A., Canto-Canche, B., Churchill, A. C. L., Conde-Ferràez, L., Cools, H. J., Coutinho, P. M., Csukai, M., Dehal, P., De Wit, P., Donzelli, B., van de Geest, H. C., van Ham, R. C. H. J., Hammond-Kosack, K. E., Henrissat, B., Kilian, A., Kobayashi, A. K., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J. P. H., Ponomarenko, A., Rudd, J. J., Salamov, A., Schmutz, J., Schouten, H. J., Shapiro, H., Stergiopoulos, I., Torriani, S. F. F., Tu, H., de Vries, R. P., Waalwijk, C., Ware, S. B., Wiebenga, A., Zwiers, L.-H., Oliver, R. P., Grigoriev, I. V., and Kema, G. H. J. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity and stealth pathogenesis. PLoS Genet. 7(6):e1002070. doi:10.1371/journal.pgen. 1002070.
17. Goodwin, S. B., van der Lee, T. A. J., Cavaletto, J. R., Hekkert, B. T. L., Crane, C. F., and Kema, G. H. J. 2007. Identification and genetic mapping of highly polymorphic microsatellite loci from and EST database of the Septoria tritici blotch pathogen Mycosphaerella graminicola. Fungal Genet. Biol. 44:398-414. (Pubitemid 46483137)
18. Grünwald, N. J., Goodwin, S. B., Milgroom, M. G., and Fry, W. E. 2003. Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738-746. (Pubitemid 36610409)
19. Hedrick, P. 2005. A standardized genetic differentiation measure. Evolution 59:1633-1638. (Pubitemid 41266769)
20. Jost, L. 2008. GST and its relatives do not measure differentiation. Mol. Ecol. 17:4015-4026.
21. Kabbage, M., Leslie, J. F., Hulbert, S. H., and Bockus, W. W. 2009. Comparison of natural populations of Mycosphaerella graminicola from single fields in Kansas and California. Physiol. Mol. Plant Pathol. 74:55-59.
22. Kabbage, M., Leslie, J. F., Zeller, K. A., Hulbert, S. H., and Bockus, W. W. 2008. Genetic diversity of Mycosphaerella graminicola, the causal agent of Septoria tritici blotch, in Kansas winter wheat. J. Agric. Food Environ. Sci. 2:1-9.
23. Kema, G. H. J., Verstappen, E. C. P., Todorova, M., and Waalwijk, C. 1996. Successful crosses and molecular trend and progeny analyses demonstrate heterothallism in Mycosphaerella graminicola. Curr. Genet. 30:251-258. (Pubitemid 26336191)
24. Kerényi, Z., Zeller, K. A., Hornok, L., and Leslie, J. F. 1999. Molecular standardization of mating type terminology in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 65:4071-4076.
25. Kraft, T., Sall T., Magnusson-Rading, I., Nilsson, N. O., and Hallden, C. 1998. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics 150:1239-1244. (Pubitemid 28510051)
26. Linde, C., Zhan, J., and McDonald, B. A. 2002. Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92:946-955.
27. McDonald, B. A., and Linde, C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-379. (Pubitemid 35235585)
28. McDonald, B. A., and Martinez, J. P. 1990. DNA restriction fragment length polymorphisms among Mycosphaerella graminicola (anamorph Septoria tritici) isolates collected from a single wheat field. Phytopathology 80:1368-1373.
29. McDonald, B. A., and McDermott, J. M. 1993. The population genetics of plant pathogenic fungi. BioScience 43:311-319.
30. Meirmans, P. G., and Hedrick, P. W. 2011. Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11:5-18.
31. Meirmans, P. G., and van Tienderen, P. H. 2004. GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4:792-794. (Pubitemid 39569241)
32. Milgroom, M. G. 1996. Recombination and the multilocus structure of fungal populations. Annu. Rev. Phytopathol. 34:457-477. (Pubitemid 26400750)
33. Murray, M. G., and Thompson, W. F. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8:4321-4325.
34. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA 70:3321-3323.
35. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-590. (Pubitemid 8396073)
36. Peakall, R., and Smouse, P. E. 2006. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288-295. (Pubitemid 43373825)
37. Razavi, M., and Hughes, G. R. 2004. Molecular variability of Mycosphaerella graminicola as detected by RAPD markers. J. Phytopathol. 152:543-548. (Pubitemid 39455190)
38. Schneider, F., Koch, G., Jung, C., and Verreet, J. A. 2001. Genotypic diversity of the wheat leaf blotch pathogen Mycosphaerella graminicola (anamorph) Septoria tritici in Germany. Eur. J. Plant Pathol. 107:285-290. (Pubitemid 32614546)
39. Selkoe, K. A., and Toonen, R. J. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9:615-629.
40. Shaw, M. W., and Royle, D. J. 1989. Airborne inoculums as a major source of Septoria tritici (Mycosphaerella graminicola) infections in winter wheat crops in the UK. Plant Pathol. 38:35-43.
41. Shi, J., Ward, R., Wang, D., and Lewis, J. 2001. Application of a high throughput, low cost, non-denaturing polyacrylamide gel system for wheat microsatellite mapping. Pages 25-30 in: National Fusarium Head Blight Forum, Erlanger, KY.
42. Sommerhalder, R. J., McDonald, B. A., and Zhan, J. 2006. The frequencies and spatial distribution of mating types in Stagonospora nodorum are consistent with recurring sexual reproduction. Phytopathology 96:234-239.
43. Stoddart, J. A., and Taylor, J. F. 1988. Genotypic diversity: estimation and prediction in samples. Genetics 118:705-711.
44. Waalwijk, C., Mendes, O., Verstappen, E. C. P., de Waard, M. A., and Kema, G. H. J. 2002. Isolation and characterization of the mating type idiomorphs from the wheat Septoria leaf blotch fungus Mycosphaerella graminicola. Fungal Genet. Biol. 35:277-286.
45. Whitlock, M. C. 2011. G'ST and D do not replace FST. Mol. Ecol. 20:1083-1091.
46. Yeh, F. C., Yang, R. C., Boyle, T. B. J., Ye, Z. H., and Mao, J. X. 1997. POPGENE, the User Friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Center, University of Alberta, Canada.
47. Zhan, J., Kema, G. H. J., Waalwijk, C., and McDonald, B. A. 2002. Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal Genet. Biol. 36:128-136. (Pubitemid 34757038)
48. Zhan, J., and McDonald, B. A. 2004. The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genet. Biol. 41:590-599. (Pubitemid 38581868)
49. Zhan, J., Mundt, C. C., Hoffer, M. E., and McDonald, B. A. 2002. Local adaptation and effect of host genotype on the evolution of virulence: An experimental test in a plant pathosystem. J. Evol. Biol. 15:634-647. (Pubitemid 34763137)
50. Zhan, J., Mundt, C. C., and McDonald, B. A. 2001. Using RFLPs to assess temporal variation and estimate the number of ascospores that initiate epidemics in field populations of Mycosphaerella graminicola. Phytopathology 91:1011-1017. (Pubitemid 32961691)
51. Zhan, J., Pettway, R. E., and McDonald, B. A. 2003. The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet. Biol. 38:286-297. (Pubitemid 36398175)
52. Zhan, J., Torriani, S. F. F., and McDonald, B. A. 2007. Significant difference in pathogenicity between MAT1-1 and MAT1-2 isolates in the wheat pathogen Mycosphaerella graminicola. Fungal Genet. Biol. 44:339-346. (Pubitemid 46509470)