, Volume 138, Issue 3, pp 313–319 | Cite as

The impact of genome defense on mobile elements in Microbotryum

  • Louise J. Johnson
  • Tatiana Giraud
  • Ryan Anderson
  • Michael E. Hood


Repeat induced point mutation (RIP), a mechanism causing hypermutation of repetitive DNA sequences in fungi, has been described as a ‘genome defense’ which functions to inactivate mobile elements and inhibit their deleterious effects on genome stability. Here we address the interactions between RIP and transposable elements in the Microbotryum violaceum species complex. Ten strains of M. violaceum, most of which belong to different species of the fungus, were all found to contain intragenomic populations of copia-like retrotransposons. Intragenomic DNA sequence variation among the copia-like elements was analyzed for evidence of RIP. Among species with RIP, there was no significant correlation between the frequency of RIP-induced mutations and inferred transposition rate based on diversity. Two strains of M. violaceum, from two different plant species but belonging to the same fungal lineage, contained copia-like elements with very low diversity, as would result from a high transposition rate, and these were also unique in showing no evidence of the hypermutation patterns indicative of the RIP genome defense. In this species, evidence of RIP was also absent from a Class II helitron-like transposable element. However, unexpectedly the absolute repetitive element load was lower than in other strains.


Anther smut Ustilago violacea Helitron Retrotransposons Copy number variation 



This work was supported by NSF award DEB-0446671 to M. E. Hood. We thank Misty Hurt for technical advice, Janis Antonovics for comments on an earlier version of this manuscript, and anonymous reviews for helpful comments.


  1. Agrawal N, Dasaradhi PVN, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev 67(4):657–688CrossRefPubMedGoogle Scholar
  2. Almaraz T, Roux C, Maumont S, Durrieu G (2002) Phylogenetic relationships among smut fungi parasitizing dicotyledons based on ITS sequence analysis. Mycol Res 106:541–548CrossRefGoogle Scholar
  3. Bestor TH (1999) Sex brings transposons and genomes into conflict. Genetica 107(1–3):289–295CrossRefPubMedGoogle Scholar
  4. Clutterbuck A (2004) MATE transposable elements in Aspergillus nidulans: evidence of repeat-induced point mutation. Fungal Genet Biol 41:308–316CrossRefPubMedGoogle Scholar
  5. Crouch JA, Glasheen BM, Giunta MA, Clarke BB, Hillman BI (2008) The evolution of transposon repeat-induced point mutation in the genome of Colletotrichum cereale: reconciling sex, recombination and homoplasy in an “asexual” pathogen. Fungal Genet Biol 45:190–206CrossRefPubMedGoogle Scholar
  6. Daboussi M-J, Capy P (2003) Transposable elements in filamentous fungi. Annu Rev Microbiol 57:275–299CrossRefPubMedGoogle Scholar
  7. Daboussi M-J, Daviere J-M, Graziani G, Langin T (2002) Evolution of the Fot1 transposons in the genus Fusarium: discontinuous distribution and epigenetic inactivation. Mol Biol Evol 19:510–520PubMedGoogle Scholar
  8. Deceliere G, Charles S, Biémont C (2005) The dynamics of transposable elements in structured populations. Genetics 169:467–474CrossRefPubMedGoogle Scholar
  9. Flavell AJ (1999) Long terminal repeat retrotransposons jump between species. Proc Natl Acad Sci USA 96(22):12211–12212CrossRefPubMedGoogle Scholar
  10. Flavell AJ, Pearce SR, Heslop-Harrison P, Kumar A (1997) The evolution of Ty1-copia retrotransposons in eukaryote genomes. Genetica 100:185–195CrossRefPubMedGoogle Scholar
  11. Galagan JA, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20(9):417–423CrossRefPubMedGoogle Scholar
  12. Garber ED, Ruddat M (1994) Genetics of Ustilago violacea. XXXII. Genetic evidence for transposable elements. Theor Appl Genet 89:838–846CrossRefGoogle Scholar
  13. Garber ED, Ruddat M (1998) Genetics of Ustilago violacea. XXXIV. Genetic evidence for a transposable element functioning during mitosis and two transposable elements functioning during meiosis. Int J Plant Sci 159:1018–1022Google Scholar
  14. Garber ED, Ruddat M (2000) Genetics of Ustilago violacea. XXXV. Transposition in haploid and diploid sporidia and germinating teliospores. Int J Plant Sci 161:227–231CrossRefPubMedGoogle Scholar
  15. Garber ED, Ruddat M (2002) Transmission genetics of Microbotryum violaceum (Ustilago violacea): a case history. Adv Appl Microbiol 51:107–127CrossRefPubMedGoogle Scholar
  16. Giraud T, Jonot O, Shykoff JA (2005) Selfing propensity under choice conditions in a parasitic fungus, Microbotryum violaceum, and parameters influencing infection success in artificial inoculations. Int J Plant Sci 166:649–657CrossRefGoogle Scholar
  17. Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME (2008) The mating system of the anther smut fungus, Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell 7:765–775CrossRefPubMedGoogle Scholar
  18. Goddard MR, Burt A (1999) Recurrent invasion and extinction of a selfish gene. PNAS USA 96(24):13880–13885CrossRefPubMedGoogle Scholar
  19. Hamann A, Feller F, Osiewacz HD (2000) The degenerate DNA transposon Pat and repeat-induced point mutation (RIP) in Podospora anserina. Mol Gen Genet 263:1061–1069CrossRefPubMedGoogle Scholar
  20. Hood ME (2005) Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124(1):1–10CrossRefPubMedGoogle Scholar
  21. Hood ME, Katawczik M, Giraud T (2005) Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170(3):1081–1089CrossRefPubMedGoogle Scholar
  22. Hurst LD (1992) Intragenomic conflict as an evolutionary force. Proc R Soc 248(1322):135–140CrossRefGoogle Scholar
  23. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y, Tosa Y, Mayama S (2002) Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field environment. Mol Microbiol 45(5):1355–1364CrossRefPubMedGoogle Scholar
  24. Johnson LJ (2007) The genome strikes back: the evolutionary importance of defence against mobile elements. Evol Biol 34:121–129CrossRefGoogle Scholar
  25. Josse T, Teysset L, Todeschini A-L, Sidor C, Anxolabéhère D, Ronsseray S (2007) Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLOS Genet 3(9):e158Google Scholar
  26. Kidwell MG, Lisch DR (2001) Transposable elements, parasitic DNA and genome evolution. Evolution 55(1):1–24PubMedGoogle Scholar
  27. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefPubMedGoogle Scholar
  28. Le Gac M, Hood ME, Fournier E, Giraud T (2007) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61:15–26CrossRefPubMedGoogle Scholar
  29. Lutz M, Piatek M, Kemler M, Chlebicki A, Oberwinkler F (2008) Anther smuts of Caryophyllaceae: molecular analyses reveal further new species. Mycol Res 112:1280–1296CrossRefPubMedGoogle Scholar
  30. Nee S, Maynard Smith J (1990) The evolutionary biology of molecular parasites. Parasitology 100:S5–S18CrossRefPubMedGoogle Scholar
  31. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  32. Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46:439–450CrossRefPubMedGoogle Scholar
  33. Yockteng R, Marthey S, Chiapello H, Gendrault A, Hood ME, Rodolphe F, Wincker P, Dossat C, Giraud T (2007) Expressed sequences tags of the anther smut fungus, Microbotryum violaceum, identify mating and pathogenicity gene. BMC Genomics 8:272CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Louise J. Johnson
    • 1
  • Tatiana Giraud
    • 2
    • 3
  • Ryan Anderson
    • 4
  • Michael E. Hood
    • 5
  1. 1.School of Biological SciencesUniversity of ReadingReadingUK
  2. 2.Ecologie, Systématique et EvolutionCentre National de la Recherche Scientifique, CNRSOrsay cedexFrance
  3. 3.Université Paris-SudOrsay cedexFrance
  4. 4.Department of BiologyUniversity of VirginiaCharlottesvilleUSA
  5. 5.Department of BiologyAmherst CollegeAmherstUSA

Personalised recommendations