Australasian Plant Pathology

, Volume 41, Issue 1, pp 41–46 | Cite as

High levels of genetic diversity and cryptic recombination is widespread in introduced Diplodia pinea populations

  • Wubetu Bihon
  • Treena Burgess
  • Bernard Slippers
  • Michael J. Wingfield
  • Brenda D. Wingfield
Article

Abstract

Introduced populations of organisms typically have reduced diversity compared to those that are native. It is, therefore, unusual that introduced populations of the fungal tree pathogen Diplodia pinea have been shown to have high levels of genetic diversity, even surpassing diversity in some native regions. This is thought to be due to multiple introductions over time or the existence of a cryptic and yet undiscovered sexual cycle. In this study, we consider whether populations of D. pinea in Southern Hemisphere countries have similar patterns of diversity, share some level of genetic identity and how they might be influenced by sexual recombination. A total of 173 isolates from Argentina, Australia, Ethiopia and South Africa were characterized using 12 microsatellite markers. The results show that all these populations have high gene and genotype diversities, with the Australian population having the lowest diversity. Very few private alleles were found, suggesting that isolates from different countries might share a source of introduction. However, based on allele distribution and frequency, each of the populations appeared to be evolving independently. The results showed that in all but the Australian population, alleles are randomly associated, suggesting that widespread sexual recombination has influenced population structure.

Keywords

Diplodia pinea Simple sequence repeat marker Genetic diversity Cryptic sex 

Notes

Acknowledgements

This research was financially supported by the DST/NRF Centre of Excellence in Tree Health Biotechnology (CTHB), members of the Tree Protection Co-operative Program (TPCP) and the International Foundation for Sciences, Stockholm, Sweden, through a grant to Wubetu Bihon.

References

  1. Agapow PM, Burt A (2000) ‘Multilocus 1.2’. Department of Biology, Imperial College, AscotGoogle Scholar
  2. Arie T, Kaneko I, Yoshida T, Noguchi M, Nomura Y, Yamaguchi I (2000) Mating-type genes from asexual phytopathogenic ascomycets Fusarium oxysprum and Alternaria alternata. Mol Plant Microbe Interact 13:1330–1339PubMedCrossRefGoogle Scholar
  3. Bihon W, Burgess T, Slippers B, Wingfield MJ, Wingfield BD (2011a) Distribution of D. pinea and its genotypic diversity within asymptomatic P. patula trees. Australas Plant Pathol 40:540–548. doi: 10.1007/s13313-011-0060-z CrossRefGoogle Scholar
  4. Bihon W, Slippers B, Burgess T, Wingfield MJ, Wingfield BD (2011b) Diverse sources of infection and cryptic recombination revealed in South African Diplodia pinea populations. Fungal Biol (submitted)Google Scholar
  5. Bihon W, Slippers B, Burgess T, Wingfield MJ, Wingfield BD (2010) Sources of Diplodia pinea endophytic infections in Pinus patula and P. radiata seedlings in South Africa. Forest Pathol. doi: 10.1111/j.1439-0329.2010.00691.x
  6. Burgess T, Wingfield BD, Wingfield MJ (2001a) Comparison of genotypic diversity in native and introduced populations of Sphaeropsis sapinea isolated from Pinus radiata. Mycol Res 105:1331–1339CrossRefGoogle Scholar
  7. Burgess T, Wingfield MJ, Wingfield BD (2001b) Simple sequence repeat markers distinguished among morphotypes of Sphaeropsis sapinea. Appl Environ Microbiol 67:354–362PubMedCrossRefGoogle Scholar
  8. Burgess TI, Wingfield MJ (2002) Quarantine is important in restricting the spread of exotic seed-borne tree pathogens in the southern hemisphere. Int Forest Rev 4:56–65Google Scholar
  9. Burgess T, Wingfield MJ, Wingfield BD (2004) Global distribution of Diplodia pinea genotypes revealed using simple sequence repeat (SSR) markers. Australas Plant Pathol 33:513–519CrossRefGoogle Scholar
  10. Feci E, Smith D, Stanosz DR (2003) Association of Sphaeropsis sapinea with insect-damaged red pine shoots and cones. Forest Pathol 33:7–13CrossRefGoogle Scholar
  11. Geiser DM, Arnold ML, Timberlake WE (1994) Sexual origins of British Aspergillus nidulans isolates. Proc Natl Acad Sci USA 91:2349–2352PubMedCrossRefGoogle Scholar
  12. Goss EM, Larsen M, Chastagner GA, Givens DR, Grunwald NJ (2009) Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Pathog 5:e1000583. doi: 10.1371/journal.ppat.1000583 PubMedCrossRefGoogle Scholar
  13. Groenewald M, Linde CC, Groenewald JZ, Crous PW (2008) Indirect evidence for sexual reproduction in Cercospora beticola populations from sugar beet. Plant Pathol 57:25–32Google Scholar
  14. Halliburton R (2004) Introduction to population genetics. Pearson Education, Inc., USAGoogle Scholar
  15. Hunter GC, van der Merwe NA, Burgess TI, Carnegie AJ, Wingfield BD, Crous PW, Wingfield MJ (2008) Global movement and population biology of Mycosphaerella nubilosa infecting leaves of cold-tolerant Eucalyptus globulus and E. nitens. Plant Pathol 57:235–242CrossRefGoogle Scholar
  16. Kohli Y, Kohn LM (1998) Random association among alleles in clonal populations of Sclerotinia sclerotiorum. Fungal Genet Biol 23:139–149PubMedCrossRefGoogle Scholar
  17. Kuck U, Poggeler S (2009) Cryptic sex in fungi. Fungal Biol Rev 23:86–90CrossRefGoogle Scholar
  18. Linde CC (2010) Population genetic analyses of plant pathogens: new challenges and opportunities. Australas Plant Pathol 39:23–28, BlackwellCrossRefGoogle Scholar
  19. McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453PubMedCrossRefGoogle Scholar
  20. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential and durable resistance. Annu Rev Phytopathol 40:349–379PubMedCrossRefGoogle Scholar
  21. McDonald BA, McDermott JM (1993) Population genetics of plant pathogenic fungi: electrophoretic markers give unprecedented precision to analyses of genetic structure of populations. Bioscience 43:311–319CrossRefGoogle Scholar
  22. Milgroom MG, Fry WE (1997) Contributions of population genetics to plant disease epidemiology and management. Adv Bot Res 24:1–30CrossRefGoogle Scholar
  23. Milgroom MG, Sotirovski K, Spica D, Davis JE, Brewer MT, Milev M, Cortesi P (2008) Clonal population structure of the chestnut blight fungus in expanding ranges in South Eastern Europe. Mol Ecol 17:4446–4458PubMedCrossRefGoogle Scholar
  24. Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall REB, Parker JM, Longcore JE, Moitz C, Briggs CJ, Taylor JW (2007) Population genetics of the from-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci USA 104:13845–13850PubMedCrossRefGoogle Scholar
  25. Nevo E (1978) Genetic variation in natural populations: patterns and theory. Theor Popul Biol 13:121–177PubMedCrossRefGoogle Scholar
  26. Palmer MA, Stewart EL, Wingfield MJ (1987) Variation among isolates of Sphaeropsis sapinea in the north central United States. Phytopathology 77:944–948CrossRefGoogle Scholar
  27. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  28. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  29. Smith H, Wingfield MJ, de Wet J, Coutinho TA (2000) Genotypic diversity of Sphaeropsis sapinea from South Africa and Northern Sumatra. Plant Dis 84:139–142CrossRefGoogle Scholar
  30. Stanosz GR, Swart WJ, Smith DR (1999) RAPD marker and isozyme characterization of Sphaeropsis sapinea from diverse coniferous hosts and locations. Mycol Res 103:1193–1202CrossRefGoogle Scholar
  31. Stoddart JA, Taylor JF (1988) Genotype diversity: estimation and prediction in samples. Genetics 118:705–711PubMedGoogle Scholar
  32. Sutton BC (1980) The Coelomycetes. Commonwealth Mycological Institute, KewGoogle Scholar
  33. Swart WJ, Knox-Davis PS, Wingfield MJ (1985) Sphaeiopsis sapinea, with special reference to its occurrence on Pinus spp. in South Africa. S Afr For J 35:1–8Google Scholar
  34. Swart WJ, Wingfield MJ (1991) Biology and control of Sphaeropsis sapinea on Pinus species in South Africa. Plant Dis 75:761–766CrossRefGoogle Scholar
  35. Taylor JW, Jacobson DJ, Fisher MC (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annu Rev Phytopathol 37:197–246PubMedCrossRefGoogle Scholar
  36. Weir BS (1997) Genetic data analysis II. Sinauer Associates Inc, SunderlandGoogle Scholar
  37. Wingfield MJ, Knox-Davies PS (1980) Association of Diplodia pinea with a root disease of pines in South Africa. Plant Dis 64:22–223Google Scholar
  38. Wingfield MJ, Slippers B, Roux J, Wingfield BD (2001) Worldwide movement of exotic forest fungi, especially in the tropics and the southern hemisphere. Bioscience 51:134–140CrossRefGoogle Scholar
  39. Wingfield MJ, Slippers B, Hurley BP, Coutinho TA, Wingfield BD, Roux J (2008) Eucalypt pests and diseases: growing threats to plantation productivity. Southern Forests 70:139–144CrossRefGoogle Scholar
  40. Yeh FC, Yang RC, Boyle T (1999) POPEGENE version 1.31 Microsoft windows based freeware for population genetic analysis. AlbertaGoogle Scholar
  41. Zhan J, McDonald BA (2004) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 41:590–599PubMedCrossRefGoogle Scholar
  42. Zwolinski JB, Swart WJ, Wingfield MJ (1990) Economic impact of a post-hail outbreak of dieback induced by Sphaeropsis sapinea. Eur J Forest Pathol 20:405–411CrossRefGoogle Scholar

Copyright information

© Australasian Plant Pathology Society Inc. 2011

Authors and Affiliations

  • Wubetu Bihon
    • 1
  • Treena Burgess
    • 1
    • 2
  • Bernard Slippers
    • 1
  • Michael J. Wingfield
    • 1
  • Brenda D. Wingfield
    • 1
  1. 1.Department of Genetics, Forestry and Agricultural Biotechnology InstituteUniversity of PretoriaPretoriaSouth Africa
  2. 2.School of Biological Sciences and BiotechnologyMurdoch UniversityPerthAustralia

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