Searching for clues of sexual reproduction in the genomes of arbuscular mycorrhizal fungi

Fungal Ecology

Volumn 6, Issue 1, 2013, Pages 44-49

  Riley, Rohan ^a   Corradi, Nicolas ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Ancient asexuals; Arbuscular mycorrhizal fungi; Comparative genomics; Mating type locus; Meiosis; Parasexuality; Sexual reproduction

Indexed keywords

ARBUSCULAR; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; FUNGI;

EID: 84871800111     PISSN: 17545048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funeco.2012.01.010     Document Type: Article

References (60)

1. Alby K., Schaefer D., Bennett R.J. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 2009, 460:890-893.
2. Angelard C., Sanders I.R. Effect of segregation and genetic exchange on arbuscular mycorrhizal fungi in colonization of roots. New Phytologist 2011, 189:652-657.
3. Bonfante P., Genre A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications 2010, 1:48.
4. Burmester A., Richter M., Schultze K., Voelz K., Schachtschabel D., Boland W., Wostemeyer J., Schimek C. Cleavage of beta-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated beta-carotene oxygenase. Fungal Genetics and Biology 2007, 44:1096-1108.
5. Butlin R., Schon I., Martens K. Asexual reproduction in nonmarine ostracods. Heredity 1998, 81:473-480.
6. Corradi N., Charest C. Some like it toxic. Molecular Ecology 2011, 20:3289-3290.
7. Corradi N., Sanders I.R. Evolution of the P-type II ATPase gene family in the fungi and presence of structural genomic changes among isolates of Glomus intraradices. BMC Evolutionary Biology 2006, 6.
8. Croll D., Giovannetti M., Koch A.M., Sbrana C., Ehinger M., Lammers P.J., Sanders I.R. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 2009, 181:924-937.
9. Croll D., Sanders I.R. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evolutionary Biology 2009, 9:13.
10. De la Providencia I.E., de Souza F.A., Fernandez F., Delmas N.S., Declerck S. Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytologist 2005, 165:261-271.
11. Den Bakker H.C., Vankuren N.W., Morton J.B., Pawlowska T.E. Clonality and recombination in the life history of an asexual arbuscular mycorrhizal fungus. Molecular Biology and Evolution 2010, 27:2474-2486.
12. Dunthorn M., Katz L.A. Secretive ciliates and putative asexuality in microbial eukaryotes. Trends in Microbiology 2010, 18:183-188.
13. Dyer P.S., O'Gorman C.M. A fungal sexual revolution: Aspergillus and Penicillium show the way. Current Opinion in Microbiology 2011, 14:649-654.
14. Giovannetti M., Azzolini D., Citernesi A.S. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Applied Environmental Microbiology 1999, 65:5571-5575.
15. Gryganskyi A.P., Lee S.C., Litvintseva A.P., Smith M.E., Bonito G., Porter T.M., Anishchenko I.M., Heitman J., Vilgalys R. Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS One 2010, 5:e15273.
16. Halary S., Malik S.B., Lildhar L., Slamovits C.H., Hijri M., Corradi N. Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biology and Evolution 2011, 3:950-958.
17. Heitman J. Sexual reproduction and the evolution of microbial pathogens. Current Biology 2006, 16:711-725.
18. Heitman J. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host and Microbe 2010, 8:86-99.
19. Hijri M., Hosny M., van Tuinen D., Dulieu H. Intraspecific ITS polymorphism in Scutellospora castanea (Glomales, Zygomycota) is structured within multinucleate spores. Fungal Genetics and Biology 1999, 26:141-151.
20. Hijri M., Sanders I.R. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 2005, 433:160-163.
21. Hull C.M., Heitman J. Fungal mating: Candida albicans flips a switch to get in the mood. Current Biology 2002, 12:R782-R784.
22. Hull C.M., Johnson A.D. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 1999, 285:1271-1275.
23. Hull C.M., Raisner R.M., Johnson A.D. Evidence for mating of the "asexual" yeast Candida albicans in a mammalian host. Science 2000, 289:307-310.
24. Humphreys C.P., Franks P.J., Rees M., Bidartondo M.I., Leake J.R., Beerling D.J. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nature Communications 2010, 1.
25. Idnurm A. Sex determination in the first-described sexual fungus. Eukaryotic Cell 2011, 10.
26. Idnurm A., Walton F.J., Floyd A., Heitman J. Identification of the sex genes in an early diverged fungus. Nature 2008, 451:193-196.
27. Jones S.K., Bennett R.J. Fungal mating pheromones: choreographing the dating game. Fungal Genetics and Biology 2011, 48:668-676.
28. Judson O.P., Normark B.B. Ancient asexual scandals. Trends in Ecology and Evolution 1996, 11:41-46.
29. Koch A.M., Croll D., Sanders I.R. Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters 2006, 9:103-110.
30. Kuhn G., Hijri M., Sanders I.R. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 2001, 414:745-748.
31. Lanfranco L., Delpero M., Bonfante P. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Molecular Ecology 1999, 8:37-45.
32. Lee S.C., Corradi N., Byrnes E.J., Torres-Martinez S., Dietrich F.S., Keeling P.J., Heitman J. Microsporidia evolved from ancestral sexual fungi. Current Biology 2008, 18:1675-1679.
33. Lee S.C., Ni M., Li W.J., Shertz C., Heitman J. The evolution of sex: a perspective from the fungal kingdom. Microbiology and Molecular Biology Reviews 2010, 74.
34. Lee S.C., Weiss L.M., Heitman J. Generation of genetic diversity in microsporidia via sexual reproduction and horizontal gene transfer. Communicative and Integative Biology 2009, 2:414-417.
35. Lin X., Hull C.M., Heitman J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 2005, 434:1017-1021.
36. Liu Y., Steenkamp E.T., Brinkmann H., Forget L., Philippe H., Lang B.F. Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evolutionary Biology 2009, 9:272.
37. Liu Y.J., Hodson M.C., Hall B.D. Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evolutionary Biology 2006, 6:74.
38. LloydMacgilp S.A., Chambers S.M., Dodd J.C., Fitter A.H., Walker C., Young J.P.W. Diversity of the ribosomal internal transcribed spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytologist 1996, 133:103-111.
39. Malik S.B., Pightling A.W., Stefaniak L.M., Schurko A.M., Logsdon J.M. An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS One 2008, 3.
40. Martin F., Kohler A., Murat C., Balestrini R., Coutinho P.M., Jaillon O., Montanini B., Morin E., Noel B., Percudani R., Porcel B., Rubini A., Amicucci A., Amselem J., Anthouard V., Arcioni S., Artiguenave F., Aury J.M., Ballario P., Bolchi A., Brenna A., Brun A., Buee M., Cantarel B., Chevalier G., Couloux A., Da Silva C., Denoeud F., Duplessis S., Ghignone S., Hilselberger B., Iotti M., Marcais B., Mello A., Miranda M., Pacioni G., Quesneville H., Riccioni C., Ruotolo R., Splivallo R., Stocchi V., Tisserant E., Viscomi A.R., Zambonelli A., Zampieri E., Henrissat B., Lebrun M.H., Paolocci F., Bonfante P., Ottonello S., Wincker P. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038.
41. Normark B.B., Judson O.P., Moran N.A. Genomic signatures of ancient asexual lineages. Biological Journal of the Linnean Society 2003, 79:69-84.
42. O'Gorman C.M., Fuller H.T., Dyer P.S. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 2009, 457:471-474.
43. Parfrey L.W., Lahr D.J.G., Katz L.A. The dynamic nature of eukaryotic genomes. Molecular Biology and Evolution 2008, 25:787-794.
44. Pawlowska T.E. Genetic processes in arbuscular mycorrhizal fungi. FEMS Microbiology Letters 2005, 251:185-192.
45. Pawlowska T.E., Taylor J.W. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 2004, 427:733-737.
46. Poggeler S. Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigates. Current Genetics 2002, 42:153-160.
47. Ramesh M.A., Malik S.B., Logsdon J.M. A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology 2005, 15:185-191.
48. Redecker D., Kodner R., Graham L.E. Glomalean fungi from the Ordovician. Science 2000, 289:1920-1921.
49. Rispail N., Di Pietro A. The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum. Molecular Plant Pathology 2010, 11:395-407.
50. Rodriguez A., Clapp J.P., Dodd J.C. Ribosomal RNA gene sequence diversity in arbuscular mycorrhizal fungi (Glomeromycota). Journal of Ecology 2004, 92:986-989.
51. Sanders I.R. Ecology and evolution of multigenomic arbuscular mycorrhizal fungi. The American Naturalist 2002, 160(Suppl. 4):S128-S141.
52. Sanders I.R. Preference, specificity and cheating in the arbuscular mycorrhizal symbiosis. Trends in Plant Science 2003, 8:143-145.
53. Sanders I.R., Croll D. Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annual Review of Genetics 2010, 44:271-292.
54. Schurko A.M., Logsdon J.M. Using a meiosis detection toolkit to investigate ancient asexual "scandals" and the evolution of sex. Bioessays 2008, 30:579-589.
55. Schurko A.M., Neiman M., Logsdon J.M. Signs of sex: what we know and how we know it. Trends in Ecology and Evolution 2009, 24:208-217.
56. Smith J.M. Evolution - contemplating life without sex. Nature 1986, 324:300-301.
57. Tisserant E., Kohler A., Dozolme-Seddas P., Balestrini R., Benabdellah K., Colard A., Croll D., Da Silva C., Gomez S.K., Koul R., Ferrol N., Fiorilli V., Formey D., Franken P., Helber N., Hijri M., Lanfranco L., Lindquist E., Liu Y., Malbreil M., Morin E., Poulain J., Shapiro H., van Tuinen D., Waschke A., Azcon-Aguilar C., Becard G., Bonfante P., Harrison M.J., Kuster H., Lammers P., Paszkowski U., Requena N., Rensing S.A., Roux C., Sanders I.R., Shachar-Hill Y., Tuskan G., Young J.P., Gianinazzi-Pearson V., Martin F. The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytologist 2012, 193:744-769.
58. Vandenkoornhuyse P., Leyval C., Bonnin I. High genetic diversity in arbuscular mycorrhizal fungi: evidence for recombination events. Heredity 2001, 87:243-253.
59. Welch D.M., Meselson M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 2000, 288:1211-1215.
60. Wong S., Fares M.A., Zimmermann W., Butler G., Wolfe K.H. Evidence from comparative genomics for a complete sexual cycle in the 'asexual' pathogenic yeast Candida glabrata. Genome Biology 2003, 4.