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.

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2013-08-01
2020-01-26
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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 Lett8:253–257 [CrossRef][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. Biotechniques4:376–378
    [Google Scholar]
  3. Burgeff H..( 1924;). Untersuchungen über Sexualität und Parasitismus bei Mucorineen.. Bot Abhandl4:5–135
    [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 Res150:63–70 [CrossRef][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 Biochem220:403–408 [CrossRef][PubMed]
    [Google Scholar]
  6. Burmester A., Wöstemeyer A., Wöstemeyer J..( 1990;). Integrative transformation of a zygomycete, Absidia glauca, with vectors containing repetitive DNA. Curr Genet17:155–161 [CrossRef]
    [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 Genet235:166–172 [CrossRef][PubMed]
    [Google Scholar]
  8. Claros M. G., Vincens P..( 1996;). Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem241:779–786 [CrossRef][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 Evol17:1769–1773 [CrossRef][PubMed]
    [Google Scholar]
  10. Doolittle W. F., Bapteste E..( 2007;). Pattern pluralism and the tree of life hypothesis. Proc Natl Acad Sci U S A104:2043–2049 [CrossRef][PubMed]
    [Google Scholar]
  11. Doolittle W. F., Zhaxybayeva O..( 2009;). On the origin of prokaryotic species. Genome Res19:744–756 [CrossRef][PubMed]
    [Google Scholar]
  12. Formosa T., Nittis T..( 1998;). Suppressors of the temperature sensitivity of DNA polymerase α mutations in Saccharomyces cerevisiae.. Mol Gen Genet257:461–468 [CrossRef][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 [CrossRef][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 Genet22:319–325 [CrossRef][PubMed]
    [Google Scholar]
  15. Heinemann J. A., Sprague G. F. Jr.( 1989;). Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature340:205–209 [CrossRef][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. Nature287:654–656 [CrossRef]
    [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 Genomics265:225–233 [CrossRef][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 Bio2:197–201 [CrossRef][PubMed]
    [Google Scholar]
  20. Keeling P. J..( 2009;). Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev19:613–619 [CrossRef][PubMed]
    [Google Scholar]
  21. Keeling P. J., Palmer J. D..( 2008;). Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet9:605–618 [CrossRef][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 Genet23:334–337 [CrossRef][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 Evol28:1057–1074 [CrossRef][PubMed]
    [Google Scholar]
  24. Lederberg J..( 1952;). Cell genetics and hereditary symbiosis. Physiol Rev32:403–430[PubMed]
    [Google Scholar]
  25. Lederberg J., Tatum E. L..( 1946;). Gene recombination in Escherichia coli.. Nature158:558 [CrossRef][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 Rev35:542–554 [CrossRef][PubMed]
    [Google Scholar]
  27. Moran N. A., Jarvik T..( 2010;). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science328:624–627 [CrossRef][PubMed]
    [Google Scholar]
  28. Ochman H., Gerber A. S., Hartl D. L..( 1988;). Genetic applications of an inverse polymerase chain reaction. Genetics120:621–623[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 Res108:1320–1326 [CrossRef][PubMed]
    [Google Scholar]
  30. Rosewich U. L., Kistler H. C..( 2000;). Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol38:325–363 [CrossRef][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 Microbiol175:1–7 [CrossRef][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.. Gene348:33–44 [CrossRef][PubMed]
    [Google Scholar]
  33. Skory C. D..( 2002;). Homologous recombination and double-strand break repair in the transformation of Rhizopus oryzae.. Mol Genet Genomics268:397–406 [CrossRef][PubMed]
    [Google Scholar]
  34. Skory C. D..( 2004;). Repair of plasmid DNA used for transformation of Rhizopus oryzae by gene conversion. Curr Genet45:302–310 [CrossRef][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. Proteomics4:1581–1590 [CrossRef][PubMed]
    [Google Scholar]
  36. Tatum E. L., Lederberg J..( 1947;). Gene recombination in the bacterium Escherichia coli.. J Bacteriol53:673–684[PubMed]
    [Google Scholar]
  37. Wöstemeyer J..( 1985;). Strain-dependent variation in ribosomal DNA arrangement in Absidia glauca.. Eur J Biochem146:443–448 [CrossRef][PubMed]
    [Google Scholar]
  38. Wöstemeyer J., Brockhausen-Rohdemann E..( 1987;). Inter-mating type protoplast fusion in the zygomycete Absidia glauca.. Curr Genet12:435–441 [CrossRef]
    [Google Scholar]
  39. Wöstemeyer A., Teepe H., Wöstemeyer J..( 1990;). Genetic interactions in somatic inter-mating type hybrids of the zygomycete Absidia glauca.. Curr Genet17:163–168 [CrossRef]
    [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 Bot73:S1243–250 [CrossRef]
    [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; [CrossRef]
    [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 Biol8:87 [CrossRef][PubMed]
    [Google Scholar]
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