1887

Abstract

Compared with prokaryotes, where horizontal gene transfer events are frequently found and can be studied in the laboratory at the mechanistic level, few systems are known that allow direct experimental access to parasexual phenomena in eukaryotes. In zygomycetes, a basal lineage of fungi, several mycoparasitic fungi are known that inevitably form a cytoplasmic continuum with their hosts during infection. We provide evidence that, corresponding to the expectation suggested by the morphology of the infection process, gene transfer occurs from the parasite to the host. For analysing this parasexual system at the DNA level, we characterized interspecific recombinants obtained by infecting a stable methionine-auxotrophic mutant with heavy rearrangements at the locus, which encodes homoserine acetyltransferase. Recipients were shown to be complemented by part of the corresponding gene from . This foreign DNA is neither integrated at the putative locus in the recipient strain nor integrated at , a locus encoding a hypothetical protein with amino acid similarity but with unknown function. Based on hybridization studies and on the phenotype of recipients that bear some mitotic instability of the acquired prototrophy, we propose that DNA is established in recipients as extrachromosomally located replicons.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066910-0
2013-08-01
2021-07-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/8/1639.html?itemId=/content/journal/micro/10.1099/mic.0.066910-0&mimeType=html&fmt=ahah

References

  1. Altincicek B., Kovacs J. L., Gerardo N. M.( 2012). Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae.. Biol Lett 8:253–257 [View Article][PubMed]
    [Google Scholar]
  2. Bullock W. O., Fernandez J. M., Short J. M.( 1987). XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection. Biotechniques 4:376–378
    [Google Scholar]
  3. Burgeff H.( 1924). Untersuchungen über Sexualität und Parasitismus bei Mucorineen.. Bot Abhandl 4:5–135
    [Google Scholar]
  4. Burmester A.( 1995). Analysis of the gene for the elongation factor 1 α from the zygomycete Absidia glauca. Use of the promoter region for constructions of transformation vectors. Microbiol Res 150:63–70 [View Article][PubMed]
    [Google Scholar]
  5. Burmester A., Czempinski K.( 1994). Sequence comparison of a segment of the gene for 3-hydroxy-3-methylglutaryl-coenzyme A reductase in zygomycetes. Eur J Biochem 220:403–408 [View Article][PubMed]
    [Google Scholar]
  6. Burmester A., Wöstemeyer A., Wöstemeyer J.( 1990). Integrative transformation of a zygomycete, Absidia glauca, with vectors containing repetitive DNA. Curr Genet 17:155–161 [View Article]
    [Google Scholar]
  7. Burmester A., Wöstemeyer A., Arnau J., Wöstemeyer J.( 1992). The SEG1 element: a new DNA region promoting stable mitotic segregation of plasmids in the zygomycete Absidia glauca.. Mol Gen Genet 235:166–172 [View Article][PubMed]
    [Google Scholar]
  8. Claros M. G., Vincens P.( 1996). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779–786 [View Article][PubMed]
    [Google Scholar]
  9. De Koning A. P., Brinkman F. S. L., Jones S. J. M., Keeling P. J.( 2000). Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis.. Mol Biol Evol 17:1769–1773 [View Article][PubMed]
    [Google Scholar]
  10. Doolittle W. F., Bapteste E.( 2007). Pattern pluralism and the tree of life hypothesis. Proc Natl Acad Sci U S A 104:2043–2049 [View Article][PubMed]
    [Google Scholar]
  11. Doolittle W. F., Zhaxybayeva O.( 2009). On the origin of prokaryotic species. Genome Res 19:744–756 [View Article][PubMed]
    [Google Scholar]
  12. Formosa T., Nittis T.( 1998). Suppressors of the temperature sensitivity of DNA polymerase α mutations in Saccharomyces cerevisiae.. Mol Gen Genet 257:461–468 [View Article][PubMed]
    [Google Scholar]
  13. Goto S., Kuwahara S.( 1969). Transmission of the R factor by conjugation from a naturally-isolated, multiple drug-resistant strain of Vibrio eltor to Shigella and Salmonella.. J Antibiot (Tokyo) 22:484–489 [View Article][PubMed]
    [Google Scholar]
  14. Hänfler J., Teepe H., Weigel C., Kruft V., Lurz R., Wöstemeyer J.( 1992). Circular extrachromosomal DNA codes for a surface protein in the (+) mating type of the zygomycete Absidia glauca.. Curr Genet 22:319–325 [View Article][PubMed]
    [Google Scholar]
  15. Heinemann J. A., Sprague G. F. Jr( 1989). Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340:205–209 [View Article][PubMed]
    [Google Scholar]
  16. Hernalsteens J.-P., van Vliet F., de Beuckeleer M., Depicker A., Engler G., Lemmers M., Holsters M., van Montagu M., Schell J.( 1980). The Agrobacterium tumefaciens Ti plasmid as a host vector system for introducing foreign DNA in plant cells. Nature 287:654–656 [View Article]
    [Google Scholar]
  17. Hohlweg U., Dörfler W.( 2001). On the fate of plant or other foreign genes upon the uptake in food or after intramuscular injection in mice. Mol Genet Genomics 265:225–233 [View Article][PubMed]
    [Google Scholar]
  18. Jeffries P., Young T. W. K.( 1994). 4. Biotrophic associations. Interfungal Parasitic Relationships103–122 Wallingford: CAB International;
    [Google Scholar]
  19. Karimi S., Wetzel J., Wöstemeyer J., Burmester A.( 2012). Transformation of the fungus Absidia glauca by complementation of a methionine-auxotrophic strain affected in the homoserine-acetyltransferase gene. FEBS Open Bio 2:197–201 [View Article][PubMed]
    [Google Scholar]
  20. Keeling P. J.( 2009). Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev 19:613–619 [View Article][PubMed]
    [Google Scholar]
  21. Keeling P. J., Palmer J. D.( 2008). Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618 [View Article][PubMed]
    [Google Scholar]
  22. Kellner M., Burmester A., Wöstemeyer A., Wöstemeyer J.( 1993). Transfer of genetic information from the mycoparasite Parasitella parasitica to its host Absidia glauca.. Curr Genet 23:334–337 [View Article][PubMed]
    [Google Scholar]
  23. Kloesges T., Popa O., Martin W., Dagan T.( 2011). Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol Biol Evol 28:1057–1074 [View Article][PubMed]
    [Google Scholar]
  24. Lederberg J.( 1952). Cell genetics and hereditary symbiosis. Physiol Rev 32:403–430[PubMed]
    [Google Scholar]
  25. Lederberg J., Tatum E. L.( 1946). Gene recombination in Escherichia coli.. Nature 158:558 [View Article][PubMed]
    [Google Scholar]
  26. Mehrabi R., Bahkali A. H., Abd-Elsalam K. A., Moslem M., Ben M’barek S., Gohari A. M., Jashni M. K., Stergiopoulos I., Kema G. H. J., de Wit P. J. G. M.( 2011). Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35:542–554 [View Article][PubMed]
    [Google Scholar]
  27. Moran N. A., Jarvik T.( 2010). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627 [View Article][PubMed]
    [Google Scholar]
  28. Ochman H., Gerber A. S., Hartl D. L.( 1988). Genetic applications of an inverse polymerase chain reaction. Genetics 120:621–623[PubMed]
    [Google Scholar]
  29. Roca M. G., Davide L. C., Davide L. M., Mendes-Costa M. C., Schwan R. F., Wheals A. E.( 2004). Conidial anastomosis fusion between Colletotrichum species. Mycol Res 108:1320–1326 [View Article][PubMed]
    [Google Scholar]
  30. Rosewich U. L., Kistler H. C.( 2000). Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38:325–363 [View Article][PubMed]
    [Google Scholar]
  31. Schilde C., Wöstemeyer J., Burmester A.( 2001). Green fluorescent protein as a reporter for gene expression in the mucoralean fungus Absidia glauca.. Arch Microbiol 175:1–7 [View Article][PubMed]
    [Google Scholar]
  32. Schultze K., Schimek C., Wöstemeyer J., Burmester A.( 2005). Sexuality and parasitism share common regulatory pathways in the fungus Parasitella parasitica.. Gene 348:33–44 [View Article][PubMed]
    [Google Scholar]
  33. Skory C. D.( 2002). Homologous recombination and double-strand break repair in the transformation of Rhizopus oryzae.. Mol Genet Genomics 268:397–406 [View Article][PubMed]
    [Google Scholar]
  34. Skory C. D.( 2004). Repair of plasmid DNA used for transformation of Rhizopus oryzae by gene conversion. Curr Genet 45:302–310 [View Article][PubMed]
    [Google Scholar]
  35. Small I., Peeters N., Legeai F., Lurin C.( 2004). Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590 [View Article][PubMed]
    [Google Scholar]
  36. Tatum E. L., Lederberg J.( 1947). Gene recombination in the bacterium Escherichia coli.. J Bacteriol 53:673–684[PubMed]
    [Google Scholar]
  37. Wöstemeyer J.( 1985). Strain-dependent variation in ribosomal DNA arrangement in Absidia glauca.. Eur J Biochem 146:443–448 [View Article][PubMed]
    [Google Scholar]
  38. Wöstemeyer J., Brockhausen-Rohdemann E.( 1987). Inter-mating type protoplast fusion in the zygomycete Absidia glauca.. Curr Genet 12:435–441 [View Article]
    [Google Scholar]
  39. Wöstemeyer A., Teepe H., Wöstemeyer J.( 1990). Genetic interactions in somatic inter-mating type hybrids of the zygomycete Absidia glauca.. Curr Genet 17:163–168 [View Article]
    [Google Scholar]
  40. Wöstemeyer J., Wöstemeyer A., Burmester A., Czempinski K.( 1995). Relationships between sexual processes and parasitic interactions in the host-pathogen system Absidia glauca-Parasitella parasitica.. Can J Bot 73:S1243–250 [View Article]
    [Google Scholar]
  41. Wöstemeyer J., Burmester A., Wöstemeyer A., Schultze K., Voigt K.( 2002). Gene transfer in the fungal host parasite system Absidia glauca-Parasitella parasitica depends on infection. Horizontal Gene Transfer, 2nd edn.241–247 Syvanen M., Kado C. I. London: Academic Press; [View Article]
    [Google Scholar]
  42. Xie J., Fu Y., Jiang D., Li G., Huang J., Li B., Hsiang T., Peng Y.( 2008). Intergeneric transfer of ribosomal genes between two fungi. BMC Evol Biol 8:87 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066910-0
Loading
/content/journal/micro/10.1099/mic.0.066910-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error