Multiple recent horizontal transfers of a large genomic region in cheese making fungi

Nature Communications

Volumn 5, Issue , 2014, Pages

  Cheeseman, Kevin ^a,b   Ropars, Jeanne ^c,d,e   Renault, Pierre ^a   Dupont, Joëlle ^c   Gouzy, Jérôme ^f,g   Branca, Antoine ^d,e   Abraham, Anne Laure ^a   Ceppi, Maurizio ^b   Conseiller, Emmanuel ^b   Debuchy, Robert ^d,f   Malagnac, Fabienne ^d,h   Goarin, Anne ^d   Silar, Philippe ^d,h   Lacoste, Sandrine ^c   Sallet, Erika ^f,g   Bensimon, Aaron ^b   Giraud, Tatiana ^d,e   Brygoo, Yves ⁱ  

^a UMR1319 MICALIS   (France)

^b Genomic Vision   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e UNIVERSITÉ PARIS SUD   (France)

^f CNRS   (France)

^g LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^h UNIVERSITÉ PARIS DESCARTES   (France)

ⁱ UMR8621 ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

PENICILLIN DERIVATIVE; FUNGAL DNA;

BIOTECHNOLOGY; EUKARYOTE; FOOD INDUSTRY; FUNGUS; GENOMICS; MILK;

ARTICLE; CHEESEMAKING; COMPARATIVE STUDY; DNA END JOINING REPAIR; FUNGAL DETECTION; FUNGAL GENE; FUNGAL STRAIN; GENE LOCUS; GENOMIC ISLAND; HORIZONTAL GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; PENICILLIUM; PENICILLIUM CAMEMBERTI; PENICILLIUM ROQUEFORTI; PENICILLIUM RUBENS; SEQUENCE ANALYSIS; CHEESE; GENETICS; MOLECULAR GENETICS;

BASE SEQUENCE; CHEESE; DNA, FUNGAL; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; MOLECULAR SEQUENCE DATA; PENICILLIUM;

EID: 84892149592     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3876     Document Type: Article

References (57)

1. Novo, M. et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc. Natl Acad. Sci. USA 106, 16333-16338 (2009).
2. Gibbons, J. G. et al. The evolutionary imprint of domestication on genome variation and function of the filamentous fungus Aspergillus oryzae. Curr. Biol. 22, 1403-1409 (2012).
3. Keeling, P. J. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr. Opin. Genet. Dev. 19, 613-619 (2009).
4. Andersson, J. O. Gene transfer and diversification of microbial eukaryotes. Annu. Rev. Microbiol. 63, 177-193 (2009).
5. Syvanen, M. Evolutionary implications of horizontal gene transfer. Annu. Rev. Genet. 46, 341-358 (2012).
6. Alsmark, C. et al. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 14, R19 (2013).
7. Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38, 953-956 (2006). (Pubitemid 44141666)
8. Temporini, E. D. & VanEtten, H. D. An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Neocosmospora boniensis. Curr. Genet. 46, 29-36 (2004). (Pubitemid 39077334)
9. Mehrabi, R. et al. Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol. Rev. 35, 542-554 (2011).
10. Slot, J. C. & Rokas, A. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr. Biol. 21, 134-139 (2011).
11. Ma, L.-J. et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373 (2010).
12. Dunning Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753-1756 (2007). (Pubitemid 47461840)
13. Yue, J., Hu, X., Sun, H., Yang, Y. & Huang, J. Widespread impact of horizontal gene transfer on plant colonization of land. Nat. Commun. 3, 1152 (2012).
14. Altincicek, B., Kovacs, J. L. & Gerardo, N. M. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol. Lett. 8, 253-257 (2012).
15. Sanders, I. R. Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol. Evol. 21, 656-658 (2006). (Pubitemid 44751273)
16. Samson, R. A. Introduction to food-and airborne fungi. pp 389, (2000).
17. Pitt, J. I. & Hocking, A. D. Fungi and Food Spoilage. Fungi food spoilage. pp 519 (Springer, 2009).
18. Van den Berg, M. et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161-1168 (2008).
19. Marcet-Houben, M. et al. Genome sequence of the necrotrophic fungus Penicillium digitatum, the main postharvest pathogen of citrus. BMC Genomics 13, 646 (2012).
20. Conti, C. & Bensimon, A. A combinatorial approach for fast, high-resolution mapping. Genomics 80, 135-137 (2002). (Pubitemid 36197953)
21. Lebofsky, R. & Bensimon, A. Single DNA molecule analysis: applications of molecular combing. Brief. Funct. Genomic. Proteomic. 1, 385-396 (2003).
22. Braumann, I., van den Berg, M. & Kempken, F. Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr. Genet. 53, 287-297 (2008).
23. Ropars, J. et al. Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti. PLoS One 7, e49665 (2012).
24. Kaiserer, L. et al. Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch. Microbiol. 180, 204-210 (2003). (Pubitemid 37102718)
25. Hegedüs, N., Sigl, C., Zadra, I., Pócsi, I. & Marx, F. The paf gene product modulates asexual development in Penicillium chrysogenum. J. Basic Microbiol. 51, 253-262 (2011).
26. Stergiopoulos, I. et al. In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins. Mol. Biol. Evol. 29, 3371-3384 (2012).
27. Jablonowski, D. & Schaffrath, R. Zymocin, a composite chitinase and tRNase killer toxin from yeast. Biochem. Soc. Trans. 35, 1533-1537 (2007).
28. Lewin, H. A., Larkin, D. M., Pontius, J. & O'Brien, S. J. Every genome sequence needs a good map. Genome Res. 19, 1925-1928 (2009).
29. Ricker, N., Qian, H. & Fulthorpe, R. R. The limitations of draft assemblies for understanding prokaryotic adaptation and evolution. Genomics 100, 167-175 (2012).
30. Alkan, C., Sajjadian, S. & Eichler, E. E. Limitations of next-generation genome sequence assembly. Nat. Methods 8, 61-65 (2011).
31. Rosewich, U. L. & Kistler, H. C. Role of horizontal gene transfer in the evolution of fungi. Annu. Rev. Phytopathol. 38, 325-363 (2000).
32. Fitzpatrick, D. A. Horizontal gene transfer in fungi. FEMS Microbiol. Lett. 329, 1-8 (2012).
33. Haas, F. L., Lein, J., Moses, A. J. & Puglisi, T. A. Heterokaryosis as a cause of culture rundown in Penicillium. Appl. Microbiol. 4, 187-195 (1956).
34. Gabriela Roca, M., Read, N. D. & Wheals, A. E. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol. Lett. 249, 191-198 (2005). (Pubitemid 41116209)
35. Neafsey, D. E. et al. Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res. 20, 938-946 (2010).
36. Ellison, C. E. et al. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc. Natl Acad. Sci. USA 108, 1-10 (2011).
37. Slot, J. C. & Hibbett, D. S. Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS One 2, e1097 (2007).
38. Rogers, S. & Bendich, A. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5, 69-76 (1985).
39. Rogers, S. & Bendich, A. in Plant Molecular Biology Manual. (eds Gelvin, S. & Schilperoot, R.) A6, 1-10 (Kluwer Academic Publishers, 1988).
40. Rogers, S. & Bendich, A. in Plant Molecular Biology Manual. (eds Gelvin, S. & Schilperoort, R. D1, 1-8 (Kluwer Academic Publishers, 1994).
41. Kapuscinski, J. DAPI: a DNA-specific fluorescent probe. Biotech. Histochem. 70, 220-233 (1995).
42. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008). (Pubitemid 351645072)
43. Schiex, T., Moisan, A. & Rouzé, P. EuGène: an eukaryotic gene finder that combines several sources of evidence. Lect. Notes Comput. Sci. 2066, 111-125 (2001). (Pubitemid 33298834)
44. Foissac, S. et al. Genome annotation in plants and fungi: EuGène as a model platform. Curr. Bioinform. 3, 87-97 (2008).
45. Quesneville, H. et al. Combined evidence annotation of transposable elements in genome sequences. PLoS Comput. Biol. 1, 166-175 (2005).
46. Ropars, J., Cruaud, C., Lacoste, S. & Dupont, J. A taxonomic and ecological overview of cheese fungi. Int. J. Food Microbiol. 155, 199-210 (2012).
47. Glass, N. & Donaldson, G. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61, 1323-1330 (1995).
48. Giraud, F. et al. Microsatellite loci to recognize species for the cheese starter and contaminating strains associated with cheese manufacturing. Int. J. Food Microbiol. 137, 204-213 (2010).
49. Michalet, X. et al. Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science 277, 1518-1523 (1997). (Pubitemid 27449242)
50. Cheeseman, K. et al. A diagnostic genetic test for the physical mapping of germline rearrangements in the susceptibility breast cancer genes BRCA1 and BRCA2. Hum. Mutat. 33, 998-1009 (2012).
51. Lebofsky, R., Heilig, R., Sonnleitner, M., Weissenbach, J. & Bensimon, A. DNA replication origin interference increases the spacing between initiation events in human cells. Mol. Biol. Cell 17, 5337-5345 (2006). (Pubitemid 44907373)
52. Hall, T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41, 95-98 (1999).
53. Jobb, G., von Haeseler, A. & Strimmer, K TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol. 4, 18 (2004).
54. Posada, D. jModelTest 0.1.1. Syst. Biol. 1, 1-23 (2008).
55. Galagan, J. E. & Selker, E. U. RIP: the evolutionary cost of genome defense. Trends Genet. 20, 417-423 (2004). (Pubitemid 39094570)
56. Thompson, J. D., Gibson, T. J. & Higgins, D. G in Curr. Protoc. Bioinforma. (John Wiley & Sons, Inc., 2002).
57. Hane, J. K. & Oliver, R. P. RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics 9, 478 (2008).