Molecular and morphological data support the existence of a sexual cycle in species of the genus Paracoccidioides

Eukaryotic Cell

Volumn 12, Issue 3, 2013, Pages 380-389

  Teixeira, Marcus de Melo ^a   Theodoro, Raquel Cordeiro ^b   Derengowski, Lorena da Silveira ^a   Nicola, André Moraes ^c   Bagagli, Eduardo ^b   Felipe, Maria Sueli ^a,c  

^a UNIVERSITY OF BRASILIA   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MATING HORMONE ALPHA FACTOR RECEPTOR; SEX PHEROMONE;

ARTICLE; ASEXUAL REPRODUCTION; CHEMISTRY; CYTOLOGY; FUNGAL GENE; FUNGAL GENOME; FUNGUS HYPHAE; FUNGUS SPORE; GENETIC TRANSCRIPTION; GENETICS; HIGH MOBILITY GROUP BOX DOMAIN; METABOLISM; PARACOCCIDIOIDES; PHYLOGENY; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

GENES, MATING TYPE, FUNGAL; GENOME, FUNGAL; HMG-BOX DOMAINS; HYPHAE; PARACOCCIDIOIDES; PHYLOGENY; RECEPTORS, MATING FACTOR; REPRODUCTION, ASEXUAL; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SEX ATTRACTANTS; SPORES, FUNGAL; TRANSCRIPTION, GENETIC;

EID: 84874533087     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05052-11     Document Type: Article

References (67)

1. Sugiyama J. 1987. Pleomorphic fungi: the diversity and its taxonomic implications. Elsevier, Amsterdam, Netherlands.
2. Untereiner WA, Scott JA, Naveau FA, Sigler L, Bachewich J, Angus A. 2004. The Ajellomycetaceae, a new family of vertebrate-associated Onygenales. Mycologia 96:812-821.
3. McDonough ES, Lewis AL. 1967. Blastomyces dermatitidis: production of the sexual stage. Science 156:528-529.
4. Kwon-Chung KJ. 1973. Studies on Emmonsiella capsulata. I. Heterothallism and development of the ascocarp. Mycologia 65:109-121.
5. Kwon-Chung KJ. 1975. Perfect state (Emmonsiella capsulata) of the fungus causing large-form African histoplasmosis. Mycologia 67:980-990.
6. Shiu PK, Glass NL. 2000. Cell and nuclear recognition mechanisms mediated by mating type in filamentous ascomycetes. Curr. Opin. Microbiol. 3:183-188.
7. Heitman J. 2006. Sexual reproduction and the evolution of microbial pathogens. Curr. Biol. 16:R711-R725.
8. Milgroom MG. 1996. Recombination and the multilocus structure of fungal populations. Annu. Rev. Phytopathol. 34:457-477.
9. Coppin E, Debuchy R, Arnaise S, Picard M. 1997. Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol. Biol. Rev. 61:411-428.
10. Fraser JA, Stajich JE, Tarcha EJ, Cole GT, Inglis DO, Sil A, Heitman J. 2007. Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. Eukaryot. Cell 6:622-629.
11. Li W, Metin B, White TC, Heitman J. 2010. Organization and evolutionary trajectory of the mating type (MAT) locus in dermatophyte and dimorphic fungal pathogens. Eukaryot. Cell 9:46-58.
12. Bagagli E, Bosco SM, Theodoro RC, Franco M. 2006. Phylogenetic and evolutionary aspects of Paracoccidioides brasiliensis reveal a long coexistence with animal hosts that explain several biological features of the pathogen. Infect. Genet. Evol. 6:344-351.
13. Franco M, Lacaz CS, Restrepo A, Del Negro G. 1993. Paracoccidioidomycosis. CRC Press, Boca Raton, FL.
14. San-Blas G, Nino-Vega G, Iturriaga T. 2002. Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med. Mycol. 40:225-242.
15. Matute DR, McEwen JG, Puccia R, Montes BA, San-Blas G, Bagagli E, Rauscher JT, Restrepo A, Morais F, Nino-Vega G, Taylor JW. 2006. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol. Biol. Evol. 23:65-73.
16. Teixeira MM, Theodoro RC, de Carvalho MJ, Fernandes L, Paes HC, Hahn RC, Mendoza L, Bagagli E, San-Blas G, Felipe MS. 2009. Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol. Phylogenet. Evol. 52:273-283.
17. Felipe MS, Torres FA, Maranhao AQ, Silva-Pereira I, Pocas-Fonseca MJ, Campos EG, Moraes LM, Arraes FB, Carvalho MJ, Andrade RV, Nicola AM, Teixeira MM, Jesuino RS, Pereira M, Soares CM, Brigido MM. 2005. Functional genome of the human pathogenic fungus Paracoccidioides brasiliensis. FEMS Immunol. Med. Microbiol. 45:369-381.
18. Fernandes L, Araujo MA, Amaral A, Reis VC, Martins NF, Felipe MS. 2005. Cell signaling pathways in Paracoccidioides brasiliensis-inferred from comparisons with other fungi. Genet. Mol. Res. 4:216-231.
19. Torres I, Garcia AM, Hernandez O, Gonzalez A, McEwen JG, Restrepo A, Arango M. 2010. Presence and expression of the mating type locus in Paracoccidioides brasiliensis isolates. Fungal Genet. Biol. 47:373-380.
20. Raeder U, Broda P. 1985. Rapid preparation of DNA from filamentous fungi. Lett. Appl. Microbiol. 1:3.
21. Loytynoja A, Goldman N. 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl. Acad. Sci. U. S. A. 102:10557-10562.
22. Swofford DL. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA.
23. Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetics analysis. Syst. Biol. 42:10.
24. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
25. Gish W, States DJ. 1993. Identification of protein coding regions by database similarity search. Nat. Genet. 3:266-272.
26. Bender A, Sprague GF, Jr. 1986. Yeast peptide pheromones, a-factor and alpha-factor, activate a common response mechanism in their target cells. Cell 47:929-937.
27. Fujimura HA. 1989. The yeast G-protein homolog is involved in the mating pheromone signal transduction system. Mol. Cell. Biol. 9:152-158.
28. Reed SI. 1991. Pheromone signaling pathways in yeast. Curr. Opin. Genet. Dev. 1:391-396.
29. Elion EA. 2001. The Ste5p scaffold. J. Cell Sci. 114:3967-3978.
30. Liao H, Thorner J. 1980. Yeast mating pheromone alpha factor inhibits adenylate cyclase. Proc. Natl. Acad. Sci. U. S. A. 77:1898-1902.
31. Singh P, Ghosh S, Datta A. 1997. A novel MAP-kinase kinase from Candida albicans. Gene 190:99-104.
32. Wong Sak Hoi J, Dumas B. 2010. Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot. Cell 9:480-485.
33. Achstetter T. 1989. Regulation of alpha-factor production in Saccharomyces cerevisiae: a-factor pheromone-induced expression of the MF alpha 1 and STE13 genes. Mol. Cell. Biol. 9:4507-4514.
34. Boyartchuk VL, Rine J. 1998. Roles of prenyl protein proteases in maturation of Saccharomyces cerevisiae a-factor. Genetics 150:95-101.
35. Powers S, Michaelis S, Broek D, Santa Anna S, Field J, Herskowitz I, Wigler M. 1986. RAM, a gene of yeast required for a functional modification of RAS proteins and for production of mating pheromone a-factor. Cell 47:413-422.
36. Strazdis JR, MacKay VL. 1982. Reproducible and rapid methods for the isolation and assay of a-factor, a yeast mating hormone. J. Bacteriol. 151: 1153-1161.
37. Bubnick M, Smulian AG. 2007. The MAT1 locus of Histoplasma capsulatum is responsive in a mating type-specific manner. Eukaryot. Cell 6:616-621.
38. Kwon-Chung KJ, Weeks RJ, Larsh HW. 1974. Studies on Emmonsiella capsulata (Histoplasma capsulatum). II. Distribution of the two mating types in 13 endemic states of the United States. Am. J. Epidemiol. 99:44-49.
39. Felipe MS, Andrade RV, Petrofeza SS, Maranhao AQ, Torres FA, Albuquerque P, Arraes FB, Arruda M, Azevedo MO, Baptista AJ, Bataus LA, Borges CL, Campos EG, Cruz MR, Daher BS, Dantas A, Ferreira MA, Ghil GV, Jesuino RS, Kyaw CM, Leitao L, Martins CR, Moraes LM, Neves EO, Nicola AM, Alves ES, Parente JA, Pereira M, Pocas-Fonseca MJ, Resende R, Ribeiro BM, Saldanha RR, Santos SC, Silva-Pereira I, Silva MA, Silveira E, Simoes IC, Soares RB, Souza DP, De-Souza MT, Andrade EV, Xavier MA, Veiga HP, Venancio EJ, Carvalho MJ, Oliveira AG, Inoue MK, Almeida NF, Walter ME, Soares CM, Brigido MM. 2003. Transcriptome characterization of the dimorphic and pathogenic fungus Paracoccidioides brasiliensis by EST analysis. Yeast 20:263-271.
40. Mandel MA, Barker BM, Kroken S, Rounsley SD, Orbach MJ. 2007. Genomic and population analyses of the mating type loci in Coccidioides species reveal evidence for sexual reproduction and gene acquisition. Eukaryot. Cell 6:1189-1199.
41. Paoletti M, Rydholm C, Schwier EU, Anderson MJ, Szakacs G, Lutzoni F, Debeaupuis JP, Latge JP, Denning DW, Dyer PS. 2005. Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr. Biol. 15:1242-1248.
42. Rydholm C, Szakacs G, Lutzoni F. 2006. Low genetic variation and no detectable population structure in Aspergillus fumigatus compared to closely related Neosartorya species. Eukaryot. Cell 5:650-657.
43. Kwon-Chung KJ, Bartlett MS, Wheat LJ. 1984. Distribution of the two mating types among Histoplasma capsulatum isolates obtained from an urban histoplasmosis outbreak. Sabouraudia 22:155-157.
44. Kwon-Chung KJ, Bennett JE. 1978. Distribution of alpha and alpha mating types of Cryptococcus neoformans among natural and clinical isolates. Am. J. Epidemiol. 108:337-340.
45. Kwon-Chung KJ, Edman JC, Wickes BL. 1992. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 60:602-605.
46. Sengupta P, Cochran BH. 1991. MAT alpha 1 can mediate gene activation by a-mating factor. Genes Dev. 5:1924-1934.
47. Yun SH, Berbee ML, Yoder OC, Turgeon BG. 1999. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc. Natl. Acad. Sci. U. S. A. 96:5592-5597.
48. Inderbitzin P, Harkness J, Turgeon BG, Berbee ML. 2005. Lateral transfer of mating system in Stemphylium. Proc. Natl. Acad. Sci. U. S. A. 102:11390-11395.
49. Lin X, Litvintseva AP, Nielsen K, Patel S, Floyd A, Mitchell TG, Heitman J. 2007. alpha AD alpha hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet. 3:1975-1990.
50. Cano MI, Cisalpino PS, Galindo I, Ramirez JL, Mortara RA, da Silveira JF. 1998. Electrophoretic karyotypes and genome sizing of the pathogenic fungus Paracoccidioides brasiliensis. J. Clin. Microbiol. 36:742-747.
51. Feitosa LS, Cisalpino PS, dos Santos MR, Mortara RA, Barros TF, Morais FV, Puccia R, da Silveira JF, de Camargo ZP. 2003. Chromosomal polymorphism, syntenic relationships, and ploidy in the pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet. Biol. 39:60-69.
52. Montoya AE, Alvarez AL, Moreno MN, Restrepo A, McEwen JG. 1999. Electrophoretic karyotype of environmental isolates of Paracoccidioides brasiliensis. Med. Mycol. 37:219-222.
53. Montoya AE, Moreno MN, Restrepo A, McEwen JG. 1997. Electrophoretic karyotype of clinical isolates of Paracoccidioides brasiliensis. Fungal Genet. Biol. 21:223-227.
54. Almeida AJ, Matute DR, Carmona JA, Martins M, Torres I, McEwen JG, Restrepo A, Leao C, Ludovico P, Rodrigues F. 2007. Genome size and ploidy of Paracoccidioides brasiliensis reveals a haploid DNA content: flow cytometry and GP43 sequence analysis. Fungal Genet. Biol. 44:25-31.
55. Li CH, Cervantes M, Springer DJ, Boekhout T, Ruiz-Vazquez RM, Torres-Martinez SR, Heitman J, Lee SC. 2011. Sporangiospore size dimorphism is linked to virulence of Mucor circinelloides. PLoS Pathog. 7:e1002086. doi:10.1371/journal.ppat.1002086.
56. Raudaskoski M, Kothe E. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryot. Cell 9:847-859.
57. Snetselaar KM. 1993. Microscopic observation of Ustilago maydis mating interactions. Exp. Mycol. 17:10.
58. Sohn KT, Yoon KS. 2002. Ultrastructural study on the cleistothecium development in Aspergillus nidulans. Mycobiology 30:10.
59. Ajello L, Cheng SL. 1967. The perfect state of Trichophyton mentagrophytes. Sabouraudia 5:230-234.
60. Grosse V, Krappmann S. 2008. The asexual pathogen Aspergillus fumigatus expresses functional determinants of Aspergillus nidulans sexual development. Eukaryot. Cell 7:1724-1732.
61. O'Gorman CM, Fuller HT, Dyer PS. 2009. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471-474.
62. Sigler L. 1996. Ajellomyces crescens sp. nov., taxonomy of Emmonsia spp., and relatedness with Blastomyces dermatitidis (teleomorph Ajellomyces dermatitidis). J. Med. Vet. Mycol. 34:303-314.
63. Schrick K, Garvik B, Hartwell LH. 1997. Mating in Saccharomyces cerevisiae: the role of the pheromone signal transduction pathway in the chemotropic response to pheromone. Genetics 147:19-32.
64. Poggeler S. 2002. Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus. Curr. Genet. 42:153-160.
65. Fisher MC, Koenig GL, White TJ, Taylor JW. 2002. Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non-California population of Coccidioides immitis. Mycologia 94:73-84.
66. Barker BM, Jewell KA, Kroken S, Orbach MJ. 2007. The population biology of coccidioides: epidemiologic implications for disease outbreaks. Ann. N. Y. Acad. Sci. 1111:147-163.
67. Anzawa K, Kawasaki M, Mochizuki T, Ishizaki H. 2010. Successful mating of Trichophyton rubrum with Arthroderma simii. Med. Mycol. 48:629-634.