Home LiteratureArticle Details
PMID: 11248064 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Genomic evidence for a complete sexual cycle in Candida albicans.

Tzung KW, Williams RM, Scherer S, Federspiel N, Jones T, Hansen N, Bivolarevic V, Huizar L, Komp C, Surzycki R, Tamse R, Davis RW, Agabian N

Abstract

Candida albicans is a diploid fungus that has become a medically important opportunistic pathogen in immunocompromised individuals. We have sequenced the C. albicans genome to 10.4-fold coverage and performed a comparative genomic analysis between C. albicans and Saccharomyces cerevisiae with the objective of assessing whether Candida possesses a genetic repertoire that could support a complete sexual cycle. Analyzing over 500 genes important for sexual differentiation in S. cerevisiae, we find many homologues of genes that are implicated in the initiation of meiosis, chromosome recombination, and the formation of synaptonemal complexes. However, others are striking in their absence. C. albicans seems to have homologues of all of the elements of a functional pheromone response pathway involved in mating in S. cerevisiae but lacks many homologues of S. cerevisiae genes for meiosis. Other meiotic gene homologues in organisms ranging from filamentous fungi to Drosophila melanogaster and Caenorhabditis elegans were also found in the C. albicans genome, suggesting potential alternative mechanisms of genetic exchange.

MeSH Terms
Animals Candida albicans/cytology,genetics,metabolism,physiology Genome, Fungal Meiosis/physiology Morphogenesis Signal Transduction Spores, Fungal
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Tzung K W
Graduate Program in Oral Biology, Department of Stomatology, University of California, San Francisco, CA 94143-0422, USA.
Williams R M
Scherer S
Federspiel N
Jones T
Hansen N
Bivolarevic V
Huizar L
Komp C
Surzycki R
Tamse R
Davis R W
Agabian N
References (71)
71 references, click to expand
  1. SPO13 negatively regulates the progression of mitotic and meiotic nuclear division in Saccharomyces cerevisiae.
    Genetics. 1994 Sep;138(1):47-60 PMID: 8001793
  2. Ustilago maydis, the delightful blight.
    Trends Genet. 1992 May;8(5):174-80 PMID: 1369743
  3. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12490-4 PMID: 8618927
  4. An atypical topoisomerase II from Archaea with implications for meiotic recombination.
    Nature. 1997 Mar 27;386(6623):414-7 PMID: 9121560
  5. Mdes, a mouse homolog of the Drosophila degenerative spermatocyte gene is expressed during mouse spermatogenesis.
    Dev Growth Differ. 1997 Jun;39(3):399-403 PMID: 9227906
  6. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  7. Nonfilamentous C. albicans mutants are avirulent.
    Cell. 1997 Sep 5;90(5):939-49 PMID: 9298905
  8. Meiosis: how could it work?
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167-74 PMID: 8710842
  9. DLH1 is a functional Candida albicans homologue of the meiosis-specific gene DMC1.
    Genetics. 1996 Jun;143(2):769-76 PMID: 8725225
  10. A Candida albicans gene encoding a DNA ligase.
    Yeast. 1996 Jul;12(9):893-8 PMID: 8840507
  11. A meiotic recombination checkpoint controlled by mitotic checkpoint genes.
    Nature. 1996 Oct 31;383(6603):840-3 PMID: 8893012
  12. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12473-7 PMID: 8901606
  13. Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13217-22 PMID: 8917571
  14. Degenerative spermatocyte, a novel gene encoding a transmembrane protein required for the initiation of meiosis in Drosophila spermatogenesis.
    Mol Gen Genet. 1996 Nov 27;253(1-2):157-65 PMID: 9003299
  15. Cloning, characterization, and localization of mouse and human SPO11.
    Genomics. 1999 Oct 15;61(2):156-69 PMID: 10534401
  16. RIM101-dependent and-independent pathways govern pH responses in Candida albicans.
    Mol Cell Biol. 2000 Feb;20(3):971-8 PMID: 10629054
  17. Transcriptional regulation of meiosis in yeast.
    Curr Opin Cell Biol. 2000 Jun;12(3):334-9 PMID: 10801467
  18. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth.
    Nature. 2000 Jul 6;406(6791):90-4 PMID: 10894548
  19. Evidence for mating of the "asexual" yeast Candida albicans in a mammalian host.
    Science. 2000 Jul 14;289(5477):307-10 PMID: 10894780
  20. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains.
    Science. 2000 Jul 14;289(5477):310-3 PMID: 10894781
  21. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes.
    Microbiol Mol Biol Rev. 2000 Sep;64(3):489-502 PMID: 10974123
  22. The pachytene checkpoint.
    Trends Genet. 2000 Sep;16(9):395-403 PMID: 10973068
  23. Candida albicans RIM101 pH response pathway is required for host-pathogen interactions.
    Infect Immun. 2000 Oct;68(10):5953-9 PMID: 10992507
  24. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  25. Candida concentrations in the vagina and their association with signs and symptoms of vaginal candidosis.
    J Med Vet Mycol. 1988;26(5):277-83 PMID: 3236147
  26. A regulatory hierarchy for cell specialization in yeast.
    Nature. 1989 Dec 14;342(6251):749-57 PMID: 2513489
  27. Binding of yeast a1 and alpha 2 as a heterodimer to the operator DNA of a haploid-specific gene.
    Nature. 1990 Oct 18;347(6294):682-5 PMID: 1977088
  28. Phylogenetic analysis of five medically important Candida species as deduced on the basis of small ribosomal subunit RNA sequences.
    J Gen Microbiol. 1991 May;137(5):1223-30 PMID: 1865186
  29. The yeast RME1 gene encodes a putative zinc finger protein that is directly repressed by a1-alpha 2.
    Genes Dev. 1991 Nov;5(11):1982-9 PMID: 1936989
  30. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1992 Mar;12(3):1078-86 PMID: 1545790
  31. Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex.
    Experientia. 1994 Mar 15;50(3):295-306 PMID: 8143803
  32. Control of meiotic gene expression in Saccharomyces cerevisiae.
    Microbiol Rev. 1994 Mar;58(1):56-70 PMID: 8177171
  33. A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina.
    Genetics. 1997 Oct;147(2):581-8 PMID: 9335595
  34. Meiotic chromosomes: it takes two to tango.
    Genes Dev. 1997 Oct 15;11(20):2600-21 PMID: 9334324
  35. A gene homologous to Saccharomyces cerevisiae SNF1 appears to be essential for the viability of Candida albicans.
    Infect Immun. 1997 Dec;65(12):4909-17 PMID: 9393775
  36. Mating types and sexual development in filamentous ascomycetes.
    Microbiol Mol Biol Rev. 1997 Dec;61(4):411-28 PMID: 9409146
  37. Reactivity in vegetative incompatibility of the HET-E protein of the fungus Podospora anserina is dependent on GTP-binding activity and a WD40 repeated domain.
    Mol Gen Genet. 1997 Nov;256(6):620-7 PMID: 9435787
  38. Pheromone-regulated genes required for yeast mating differentiation.
    J Cell Biol. 1998 Feb 9;140(3):461-83 PMID: 9456310
  39. Base-calling of automated sequencer traces using phred. I. Accuracy assessment.
    Genome Res. 1998 Mar;8(3):175-85 PMID: 9521921
  40. Base-calling of automated sequencer traces using phred. II. Error probabilities.
    Genome Res. 1998 Mar;8(3):186-94 PMID: 9521922
  41. Consed: a graphical tool for sequence finishing.
    Genome Res. 1998 Mar;8(3):195-202 PMID: 9521923
  42. Asexual sporulation in Aspergillus nidulans.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):35-54 PMID: 9529886
  43. Molecular genetics of mating recognition in basidiomycete fungi.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):55-70 PMID: 9529887
  44. Cell wall and secreted proteins of Candida albicans: identification, function, and expression.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):130-80 PMID: 9529890
  45. The processing of yeast pheromones.
    Semin Cell Dev Biol. 1998 Feb;9(1):19-30 PMID: 9572110
  46. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis.
    Cell. 1998 May 1;93(3):349-59 PMID: 9590170
  47. Yeast dom34 mutants are defective in multiple developmental pathways and exhibit decreased levels of polyribosomes.
    Genetics. 1998 May;149(1):45-56 PMID: 9584085
  48. Recombination at work for meiosis.
    Curr Opin Genet Dev. 1998 Apr;8(2):200-11 PMID: 9610411
  49. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80.
    Mol Cell. 1998 Apr;1(5):685-96 PMID: 9660952
  50. Snf1 kinase connects nutritional pathways controlling meiosis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1998 Aug;18(8):4548-55 PMID: 9671464
  51. The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes.
    Cell. 1998 Aug 7;94(3):375-86 PMID: 9708739
  52. An automated hydrodynamic process for controlled, unbiased DNA shearing.
    Genome Res. 1998 Aug;8(8):848-55 PMID: 9724331
  53. The control of filamentous differentiation and virulence in fungi.
    Trends Cell Biol. 1998 Sep;8(9):348-53 PMID: 9728395
  54. Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae.
    Science. 1998 Sep 18;281(5384):1854-7 PMID: 9743499
  55. The transcriptional program of sporulation in budding yeast.
    Science. 1998 Oct 23;282(5389):699-705 PMID: 9784122
  56. MAP kinase pathways in the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1264-300 PMID: 9841672
  57. Fusion of a fission yeast.
    Yeast. 1998 Dec;14(16):1529-66 PMID: 9885154
  58. Roles of the DNA mismatch repair and nucleotide excision repair proteins during meiosis.
    Cell Mol Life Sci. 1999 Mar;55(3):437-49 PMID: 10228557
  59. An automated sample preparation system for large-scale DNA sequencing.
    Genome Res. 1999 May;9(5):457-62 PMID: 10330125
  60. MOD-D, a Galpha subunit of the fungus Podospora anserina, is involved in both regulation of development and vegetative incompatibility.
    Genetics. 1999 Jun;152(2):519-28 PMID: 10353896
  61. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  62. Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions.
    Eur J Biochem. 1999 Jul;263(1):6-13 PMID: 10429180
  63. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans.
    Science. 1999 Aug 20;285(5431):1271-5 PMID: 10455055
  64. Adhesins in Candida albicans.
    Curr Opin Microbiol. 1999 Aug;2(4):353-7 PMID: 10458989
  65. Signal transduction cascades regulating mating, filamentation, and virulence in Cryptococcus neoformans.
    Curr Opin Microbiol. 1999 Aug;2(4):358-62 PMID: 10458985
  66. Whose end is destruction: cell division and the anaphase-promoting complex.
    Genes Dev. 1999 Aug 15;13(16):2039-58 PMID: 10465783
  67. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1.
    Mol Cell Biol. 1996 May;16(5):2518-26 PMID: 8628320
  68. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7327-31 PMID: 8692992
  69. Inactivation of the Podospora anserina vegetative incompatibility locus het-c, whose product resembles a glycolipid transfer protein, drastically impairs ascospore production.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5927-31 PMID: 8016091
  70. Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle.
    Genes Dev. 1994 Jun 15;8(12):1367-78 PMID: 7926737
  71. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog.
    Science. 1994 Dec 9;266(5191):1723-6 PMID: 7992058
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-03-13
Pages
3249-53
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC30639
Subset
IM
Grants
NIDCR NIH HHS · P01DE07946 · United States
NIDCR NIH HHS · DE12302-02S2 · United States
NIDCR NIH HHS · P01 DE007946 · United States
NIDCR NIH HHS · R01DE12940-01 · United States
NHGRI NIH HHS · HG01633 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]