Genome Plasticity in Candida albicans

Claude Pujol; David R. Soll

doi:10.1128/9781555817213.ch18

Chapter 18 : Genome Plasticity in Candida albicans

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Biology, The University of Iowa, Iowa City, IA 52242; 2: Department of Biology, The University of Iowa, Iowa City, IA 52242

Content Type: Monograph

Publication Year: 2012

Category: Microbial Genetics and Molecular Biology; Genomics and Bioinformatics

Book DOI: 10.1128/9781555817213

Chapter DOI: 10.1128/9781555817213.ch18

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Genome Plasticity in Candida albicans, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817213/9781555817084_Chap18-1.gif /docserver/preview/fulltext/10.1128/9781555817213/9781555817084_Chap18-2.gif

Abstract:

This chapter describes the different mechanisms of genome plasticity in Candida albicans and their impact on phenotypic plasticity, with an emphasis on recent advances in antifungal drug resistance. The average divergence between C. albicans genetic groups is approximately 2 million years. As a consequence, the recombination and genetic exchanges are most likely due to ancient mating events in C. albicans and not due to recent mating events. The requirement of sex to repair DNA damage may be moot in a diploid because sequences on homologous chromosomes can be used as templates to repair DNA breaks by an effective homologous recombination mechanism. The chapter gives a brief overview of some of the hypotheses that may particularly apply to C. albicans. A source of genome plasticity associated with recombination at MRS loci is chromosome translocation. The possibility exists that recombinations at the MRS can alter its structure and affect filamentation. In conclusion, the development of resistance to fluconazole can involve mutations at TAC1 and ERG11, as well as several genome plasticity events leading to loss of eterozygosity (LOH) and aneuploidy that affect these two genes as well as additional genes on chromosome 5.

Citation: Pujol C, Soll D. 2012. Genome Plasticity in Candida albicans, p 303-325. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch18

Key Concept Ranking

Genetic Recombination: 0.44671315
Multilocus Sequence Typing: 0.4092549

0.44671315

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555817213.chap18

1. Aanen, D. K.,, and R. F. Hoekstra,. 2007. Why sex is good: on fungi and beyond, p. 527– 534. In J. Heitman,, J. W. Kronstad,, J. W. Taylor,, and L. A. Casselton (ed.), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC.

2. Akins, R. A. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43: 285– 318.

3. Andaluz, E.,, J. Gómez-Raja,, B. Hermosa,, T. Ciudad,, E. Rustchenko,, R. Calderone,, and G. Larriba. 2007. Loss and fragmentation of chromosome 5 are major events linked to the adaptation of rad52-ΔΔ strains of Candida albicans to sorbose. Fungal Genet. Biol. 44: 789– 798.

4. Anderson, J. B.,, C. Wickens,, M. Khan,, L. E. Cowen,, N. Federspiel,, T. Jones,, and L. M. Kohn. 2001. Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J. Bacteriol. 183: 865– 872.

5. Asakura, K.,, S. Iwaguchi,, M. Homma,, T. Sukai,, K. Higashide,, and K. Tanaka. 1991. Electrophoretic karyotypes of clinically isolated yeasts of Candida albicans and C. glabrata. J. Gen. Microbiol. 137: 2531– 2538.

6. Barton, R. C.,, and S. Scherer. 1994. Induced chromosome rearrangements and morphologic variation in Candida albicans. J. Bacteriol. 176: 756– 763.

7. Barton, R. C.,, A. van Belkum,, and S. Scherer. 1995. Stability of karyotype in serial isolates of Candida albicans from neutropenic patients. J. Clin. Microbiol. 33: 794– 796.

8. Bennett, R. J.,, and A. D. Johnson. 2003. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 22: 2505– 2515.

9. Bennett, R. J.,, M. A. Uhl,, M. G. Miller,, and A. D. Johnson. 2003. Identification and characterization of a Candida albicans mating pheromone. Mol. Cell. Biol. 23; 8189– 8201.

10. Birdsell, J.,, and C. Wills. 1996. Significant competitive advantage conferred by meiosis and syngamy in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93: 908– 912.

11. Blignaut, E.,, C. Pujol,, S. Lockhart,, S. Joly,, and D. R. Soll. 2002. Ca3 fingerprinting of Candida albicans isolates from human immunodeficiency virus-positive and healthy individuals reveals a new clade in South Africa. J. Clin. Microbiol. 40: 826– 836.

12. Bougnoux, M.-E.,, C. Pujol,, D. Diogo,, C. Bouchier,, D. R. Soll,, and C. d’Enfert. 2008. Mating is rare within as well as between clades of the human pathogen Candida albicans. Fungal Genet. Biol. 45: 221– 231.

13. Bougnoux, M.-E.,, D. Diogo,, C. Pujol,, D. R. Soll,, and C. d’Enfert,. 2007. Molecular epidemiology and population dynamics in Candida albicans, p. 51– 70. In C. d’Enfert, and B. Hube (ed.), Candida: Comparative and Functional Genomics. Caister Academic Press, Norwich, United Kingdom.

14. Bougnoux, M.-E.,, D. Diogo,, N. François,, B. Sendid,, S. Veirmeire,, J. F. Colombel,, C. Bouchier,, H. Van Kruiningen,, C. d’Enfert,, and D. Poulain. 2006. Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J. Clin. Microbiol. 44: 1810– 1820.

15. Bulik, C. C.,, J. D. Sobel,, and M. D. Nailor. 2011. Susceptibility profile of vaginal isolates of Candida albicans prior to and following fluconazole introduction—impact of two decades. Mycoses 54: 34– 38.

16. Butler, G.,, M. D. Rasmussen,, M. F. Lin,, M. A. Santos,, S. Sakthikumar,, C. A. Munro,, E. Rheinbay,, M. Grabherr,, A. Forche,, J. L. Reedy,, I. Agrafioti,, M. B. Arnaud,, S. Bates,, A. J. Brown,, S. Brunke,, M. C. Costanzo,, D. A. Fitzpatrick,, P. W. de Groot,, D. Harris,, L. L. Hoyer,, B. Hube,, F. M. Klis,, C. Kodira,, N. Lennard,, M. E. Logue,, R. Martin,, A. M. Neiman,, E. Nikolaou,, M. A. Quail,, J. Quinn,, M. C. Santos,, F. F. Schmitzberger,, G. Sherlock,, P. Shah,, K. A. Silverstein,, M. S. Skrzypek,, D. Soll,, R. Staggs,, I. Stansfield,, M. P. Stumpf,, P. E. Sudbery,, T. Srikantha,, Q. Zeng,, J. Berman,, M. Berriman,, J. Heitman,, N. A. Gow,, M. C. Lorenz,, B. W. Birren,, M. Kellis,, and C. A. Cuomo. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657– 662.

17. Chen, X.,, B. B. Magee,, D. Dawson,, P. T. Magee,, and C. A. Kumamoto. 2004. Chromosome 1 trisomy compromises the virulence of Candida albicans. Mol. Microbiol. 51: 551– 565.

18. Chibana, H.,, and P. T. Magee. 2009. The enigma of the major repeat sequence of Candida albicans. Future Microbiol. 4: 171– 179.

19. Chibana, H.,, J. L. Beckerman,, and P. T. Magee. 2000. Fine-resolution physical mapping of genomic diversity in Candida albicans. Genome Res. 10: 1865– 1877.

20. Chindamporn, A.,, Y. Nakagawa,, I. Mizuguchi,, H. Chibana,, M. Doi,, and K. Tanaka. 1998. Repetitive sequences (RPS) in the chromosomes of Candida albicans are sandwiched between two novel stretches, HOK and RB2, common to each chromosome. Microbiology 144: 849– 857.

21. Chu, W. S.,, B. B. Magee,, P. T. Magee. 1993. Construction of an SfiI macrorestriction map of the Candida albicans genome. J. Bacteriol. 175: 6637– 6651.

22. Ciudad, T.,, E. Andaluz,, O. Steinberg-Neifach,, N. Lue,, N. Gow,, R. Calderone,, and G. Larriba. 2004. Homologous recombination in Candida albicans: role of CaRad52p in DNA repair, integration of linear DNA fragments and telomere length. Mol. Microbiol. 53: 1177– 1194.

23. Coste, A.,, A. Selmecki,, A. Forche,, D. Diogo,, M.-E. Bougnoux,, C. d’Enfert,, J. Berman,, and D. Sanglard. 2007. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot. Cell 6: 1889– 1904.

24. Coste, A. T.,, M. Karababa,, F. Ischer,, J. Bille,, and D. Sanglard. 2004. TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot. Cell 3: 1639– 1652.

25. Coste, A.,, V. Turner,, F. Ischer,, J. Morschhäuser,, A. Forche,, A. Selmecki,, J. Berman,, J. Bille,, and D. Sanglard. 2006. A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at Chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172: 2139– 2156.

26. Cowen, L. E.,, C. Sirjusingh,, R. C. Summerbell,, S. Walmsley,, S. Richardson,, L. M. Kohn,, and J. B. Anderson. 1999. Multilocus genotypes and DNA fingerprints do not predict variation in azole resistance among clinical isolates of Candida albicans. Antimicrob. Agents Chemother. 43: 2930– 2938.

27. Daniels, K. J.,, T. Srikantha,, S. R. Lockhart,, C. Pujol,, and D. R. Soll. 2006. Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J. 25: 2240– 2252.

28. Dignard, D.,, A. L. El-Naggar,, M. E. Logue,, G. Butler,, and M. Whiteway. 2007. Identification and characterization of MFA1, the gene encoding Candida albicans a-factor pheromone. Eukaryot. Cell 6: 487– 494.

29. Diogo, D.,, C. Bouchier,, C. d’Enfert,, and M.-E. Bougnoux. 2009. Loss of heterozygosity in commensal isolates of the asexual diploid yeast Candida albicans. Fungal Genet. Biol. 46: 159– 168.

30. Dodgson, A. R.,, K. J. Dodgson,, C. Pujol,, M. A. Pfaller,, and D. R. Soll. 2004. Clade-specific flucytosine resistance is due to a single nucleotide change in the FUR1 gene of Candida albicans. Antimicrob. Agents Chemother. 48: 2223– 2227.

31. Doi, M.,, M. Homma,, A. Chindamporn,, and K. Tanaka. 1992. Estimation of chromosome number and size by pulsed-field gel electrophoresis (PFGE) in medically important Candida species. J. Gen. Microbiol. 138: 2241– 2251.

32. Doi, M.,, M. Homma,, S. I. Iwaguchi,, K. Horibe,, and K. Tanaka. 1994. Strain relatedness of Candida albicans strains isolated from children with leukemia and their bedside parent. J. Clin. Microbiol. 32: 2253– 2259.

33. Dumitru, R.,, D. H. M. L. P. Navarathna,, C. P. Semighini,, C. G. Elowsky,, R. V. Dumitru,, D. Dignard,, M. Whiteway,, A. L. Atkin,, and K. W. Nickerson. 2007. In vivo and in vitro anaerobic mating in Candida albicans. Eukaryot. Cell 6: 465– 472.

34. Fischer, G.,, E. P. C. Rocha,, F. Brunet,, M. Vergassola,, and B. Dujon. 2006. Highly variable rates of genome rearrangements between hemiascomycetous yeast lineages. PLoS Genet. 2: e32.

35. Fonzi, W. A.,, and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717– 728.

36. Forche, A.,, K. Alby,, D. Schaefer,, A. D. Johnson,, J. Berman,, and R. J. Bennett. 2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 6: e110.

37. Forche, A.,, G. Schönian,, Y. Gräser,, R. Vilgalys,, and T. G. Mitchell. 1999. Genetic structure of typical and atypical populations of Candida albicans from Africa. Fungal Genet. Biol. 28: 107– 125.

38. Gee, S. G.,, S. Joly,, D. R. Soll,, J. F. G. M. Meis,, P. E. Verweij,, I. Polacheck,, D. J. Sullivan,, and D. C. Coleman. 2002. Identification of four distinct genotypes of Candida dubliniensis and detection of microevolution in vitro and in vivo. J. Clin. Microbiol. 40: 556– 574.

39. Goddard, M. R., 2007. Why bother with sex? Answers from experiments with yeast and other organisms, p. 489– 506. In J. Heitman,, J. W. Kronstad,, J. W. Taylor,, and L. A. Casselton (ed.), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC.

40. Goodwin, T. J. D.,, and R. T. M. Poulter. 2000. Multiple LTR-retrotransposon families in the asexual yeast Candida albicans. Genome Res. 10: 174– 191.

41. Goodwin, T. J. D.,, J. E. Ormandy,, and R. T. M. Poulter. 2001. L1-like non-LTR retrotransposons in the yeast Candida albicans. Curr. Genet. 39: 83– 91.

42. Goodwin, T. J. D.,, J. N. Busby,, and R. T. M. Poulter. 2007. A yeast model for target-primed (non-LTR) retrotransposition. BMC Genomics 8: e263.

43. Gräser, Y.,, M. Volovsek,, J. Arrington,, G. Schönian,, W. Presber,, T. G. Mitchell,, and R. Vilgalys. 1996. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc. Natl. Acad. Sci. USA 93: 12473– 12477.

44. Hilton, C.,, D. Markie,, B. Corner,, E. Rikkerink,, and R. Poulter. 1985. Heat shock induces chromosome loss in the yeast Candida albicans. Mol. Gen. Genet. 200: 162– 168.

45. Holmes, A. R.,, S. Tsao,, S.-W. Ong,, E. Lamping,, K. Niimi,, B. C. Monk,, M. Niimi,, A. Kaneko,, B. R. Holland,, J. Schmid,, and R. D. Cannon. 2006. Heterozygosity and functional allelic variation in the Candida albicans efflux pump genes CDR1 and CDR2. Mol. Microbiol. 62: 170– 186.

46. Hoyer, L. L. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9: 176– 180.

47. Huang, G.,, H. Wang,, S. Chou,, X. Nie,, J. Chen,, and H. Liu. 2006. Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc. Natl. Acad. Sci. USA 103: 12813– 12818.

48. Huang, G.,, T. Srikantha,, N. Sahni,, S. Yi,, and D. R. Soll. 2009. CO 2 regulates white-to-opaque switching in Candida albicans. Curr. Biol. 19: 330– 334.

49. Hull, C. M.,, and A. D. Johnson. 1999. Identifcation of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285: 1271– 1275.

50. Hull, C. M.,, R. M. Raisner,, and A. D. Johnson. 2000. Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science 289: 307– 310.

51. Ibrahim, A. S.,, B. B. Magee,, D. C. Sheppard,, M. Yang,, S. Kauffman,, J. Becker,, J. E. Edwards, Jr.,, and P. T. Magee. 2005. Effects of ploidy and mating type on virulence of Candida albicans. Infect. Immun. 73: 7366– 7374.

52. Iwaguchi, S.-I.,, M. Sato,, B. B. Magee,, P. T. Magee,, K. Makimura, and T Suzuki. 2001. Extensive chromosome translocation in a clinical isolate showing the distinctive carbohydrate assimilation profile from a candidiasis patient. Yeast 18: 1035– 1046.

53. Iwaguchi, S.,, M. Homma,, and K. Tanaka. 1990. Variation in the electrophoretic karyotype analysed by the assignment of DNA probes in Candida albicans. J. Gen. Microbiol. 136: 2433– 2442.

54. Iwaguchi, S.,, M. Homma,, and K. Tanaka. 1992. Clonal variation of chromosome size derived from the rDNA cluster region in Candida albicans. J. Gen. Microbiol. 138: 1177– 1184.

55. Iwaguchi, S.,, M. Suzuki,, N. Sakai,, Y. Nakagawa,, P. T. Magee,, and T. Suzuki. 2004. Chromosome translocation induced by the insertion of the URA blaster into the major repeat sequence (MRS) in Candida albicans. Yeast 21: 619– 634.

56. Jacobsen, M. D.,, A. D Duncan,, J. Bain,, E. M. Johnson,, J. R. Naglik,, D. J. Shaw,, N. A. R. Gow,, and F. C. Odds. 2008a. Mixed Candida albicans strain populations in colonized and infected mucosal tissues. FEMS Yeast Res. 8: 1334– 1338.

57. Jacobsen, M. D.,, A. M. J. Rattray,, N. A. Gow,, F. C. Odds,, and D. J. Shaw. 2008b. Mitochondrial haplotypes and recombination in Candida albicans. Med. Mycol. 46: 647– 654.

58. Janbon, G.,, F. Sherman,, and E. Rustchenko. 1998. Monosomy of a specific chromosome determines L-sorbose utilization: a novel regulatory mechanism in Candida albicans. Proc. Natl. Acad. Sci. USA 95: 5150– 5155.

59. Joly, S.,, C. Pujol,, and D. R. Soll. 2002. Microevolutionary changes and chromosomal translocations are more frequent at RPS loci in Candida dubliniensis than in Candida albicans. Infect. Genet. Evol. 2: 19– 37.

60. Joly, S.,, C. Pujol,, M. Rysz,, K. Vargas,, and D. R. Soll. 1999. Development and characterization of complex DNA fingerprinting probes for the infectious yeast Candida dubliniensis. J. Clin. Microbiol. 37: 1035– 1044.

61. Jones, T.,, N. A. Federspiel,, H. Chibana,, J. Dungan,, S. Kalman,, B. B. Magee,, G. Newport,, Y. R. Thorstenson,, N. Agabian,, P. T. Magee,, R. W. Davis,, and S. Scherer. 2004. The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 101: 7329– 7334.

62. Kanbe, T.,, T. Arishima, T Horii, and A. Kibuchi. 2003. Improvement of PCR-based identification targeting the DNA topoisomerase II gene to determine major species of the opportunistic fungi Candida and Aspergillus fumigatus. Microbiol. Immunol. 47: 631– 638.

63. Kvaal, C. A.,, T. Srikantha,, and D. R. Soll. 1997. Misexpression of the white-phase-specific gene WH11 in the opaque phase of Candida albicans affects switching and virulence. Infect. Immun. 65: 4468– 4475.

64. Kvaal, C.,, S. A. Lachke,, T. Srikantha,, K. Daniels,, J. McCoy,, and D. R. Soll. 1999. Misexpression of the opaque-phase-specific gene PEP1 ( SAP1) in the white phase of Candida albicans confers increased virulence in a mouse model of cutaneous infection. Infect. Immun. 67: 6652– 6662.

65. Lasker, B. A.,, G. F. Carle,, G. S. Kobayashi,, and G. Medoff. 1989. Comparison of the separation of Candida albicans chromosome-sized DNA by pulsed-field gel electrophoresis techniques. Nucleic Acids Res. 17: 3783– 3793.

66. Legrand, M.,, A. Forche,, A. Selmecki,, C. Chan,, D. T. Kirkpatrick,, and J. Berman. 2008. Haplotype mapping of a diploid non-meiotic organism using existing and induced aneuploidies. PLoS Genet. 4: e1.

67. Legrand, M.,, P. Lephart,, A. Forche,, F.-M. C. Mueller,, T. Walsh,, P. T. Magee,, and B. B. Magee. 2004. Homozygosity at the MTL locus in clinical strains of Candida albicans: karyotypic rearrangements and tetraploid formation. Mol. Microbiol. 52: 1451– 1462.

68. Lephart, P. R.,, and P. T. Magee. 2006. Effect of the major repeat sequence on mitotic recombination in Candida albicans. Genetics 174: 1737– 1744.

69. Lephart, P. R.,, H. Chibana,, and P. T. Magee. 2005. Effect of the major repeat sequence on chromosome loss in Candida albicans. Eukaryot. Cell 4: 733– 741.

70. Lockhart, S. R.,, B. Reed,, and D. R. Soll. 1996. Most frequent scenario for recurrent Candida vaginitis is strain maintenance with “substrain shuffling”: demonstration by sequential DNA fingerprinting with probes Ca3, C1, and CARE2. J. Clin. Microbiol. 34: 767– 777.

71. Lockhart, S. R.,, C. Pujol,, K. J. Daniels,, M. G. Miller,, A. D. Johnson,, M. A. Pfaller,, and D. R. Soll. 2002. In Candida albicans, white-opaque switchers are homozygous for mating type. Genetics 162: 737– 745.

72. Lockhart, S. R.,, J. J. Fritch,, A. S. Meier,, K. Schröppel,, T. Srikantha,, R. Galask,, and D. R. Soll. 1995. Colonizing populations of Candida albicans are clonal in origin but undergo microevolution through C1 fragment reorganization as demonstrated by DNA fingerprinting and C1 sequencing. J. Clin. Microbiol. 33: 1501– 1509.

73. Lockhart, S. R.,, K. J. Daniels,, R. Zhao,, D. Wessels,, and D. R. Soll. 2003a. Cell biology of mating in Candida albicans. Eukaryot. Cell 2: 49– 61.

74. Lockhart, S. R.,, R. Zhao,, K. J. Daniels,, and D. R. Soll. 2003b. a-pheromone-induced “shmooing” and gene regulation require white-opaque switching during Candida albicans mating. Eukaryot. Cell 2: 847– 855.

75. Lockhart, S. R.,, W. Wu,, J. B. Radke,, R. Zhao,, and D. R. Soll. 2005. Increased virulence and competitive advantage of a/a over a/a or a/a offspring conserves the mating system of Candida albicans. Genetics 169: 1883– 1890.

76. Lott, T. J.,, R. E. Fundyga,, R. J. Kuykendall,, and J. Arnold. 2005. The human commensal yeast, Candida albicans, has an ancient origin. Fungal Genet. Biol. 42: 444– 451.

77. Magee, B. B.,, and P. T. Magee. 1987. Electrophoretic karyotypes and chromosome numbers in Candida species. J. Gen. Microbiol. 133: 425– 430.

78. Magee, B. B.,, and P. T. Magee. 1997. WO-2, a stable aneuploid derivative of Candida albicans strain WO-1, can switch from white to opaque and form hyphae. Microbiology 143: 289– 295.

79. Magee, B. B.,, M. D. Sanchez,, D. Saunders,, D. Harris,, M. Berriman,, and P. T. Magee. 2008. Extensive chromosome rearrangements distinguish the karyotype of the hypovirulent species Candida dubliniensis from the virulent Candida albicans. Fungal Genet. Biol. 45: 338– 350.

80. McManus, B. A.,, D. C. Coleman,, G. Moran,, E. Pinjon,, D. Diogo,, M.-E. Bougnoux,, S. Borecká-Melkusova,, H. Bujdákova,, P. Murphy,, C. d’Enfert,, and D. J. Sullivan. 2008. Multilocus sequence typing reveals that the population structure of Candida dubliniensis is significantly less divergent than that of Candida albicans. J. Clin. Microbiol. 46: 652– 664.

81. Miller, M. G.,, and A. D. Johnson. 2002. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110: 293– 302.

82. Mishra, P. K.,, M. Baum,, and J. Carbon. 2007. Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol. Genet. Genomics 278: 455– 465.

83. Navarro-Garcia, F.,, R. M. Pérez-Diaz,, B. B. Magee,, J. Pla,, C. Nombela,, and P. Magee. 1995. Chromosome reorganization in Candida albicans 1001 strain . J. Med. Vet. Mycol. 33: 361– 366.

84. Odds, F. C.,, M.-E. Bougnoux,, D. J. Shaw,, J. M. Bain,, A. D. Davidson,, D. Diogo,, M. D. Jacobsen,, M. Lecomte,, S.-Y. Li,, A. Tavanti,, M. C. J. Maiden,, N. A. R. Gow,, and C. d’Enfert. 2007. Molecular phylogenetics of Candida albicans. Eukaryot. Cell 6: 1041– 1052.

85. Oh, S.-H.,, G. Cheng,, J. A. Nuessen,, R. Jajko,, K. M. Yeater,, X. Zhao,, C. Pujol,, D. R. Soll,, and L. L. Hoyer. 2005. Functional specificity of Candida albicans Als3p proteins and clade specificity of ALS3 alleles discriminated by the number of copies of the tandem repeat sequence in the central domain. Microbiology 151: 673– 681.

86. Olaiya, A. F.,, and S. J. Sogin. 1979. Ploidy determination of Candida albicans. J. Bacteriol. 140: 1043– 1049.

87. Perea, S.,, J. L. López-Ribot,, W. R. Kirkpatrick,, R. K. McAtee,, R. A. Santillán,, M. Martínez,, D. Calabrese,, D. Sanglard,, and T. F. Patterson. 2001. Prevalence of molecular mechanisms of resistance to azole antifungal agents in Candida albicans strains displaying high-level fluconazole resistance isolated from human immunodeficiency virus-infected patients. Antimicrob. Agents Chemother. 45: 2676– 2684.

88. Perepnikhatka, V.,, F. J. Fischer,, M. Niimi,, R. A. Baker,, R. D. Cannon,, Y.-K. Wang,, F. Sherman,, and E. Rustchenko. 1999. Specific chromosome alterations in fluconazole-resistant mutants of Candida albicans. J. Bacteriol. 181: 4041– 4049.

89. Pfaller, M. A.,, and D. J. Diekema. 2004. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin. Microbiol. Infect. 10( Suppl. 1): 11– 23.

90. Pujol, C.,, A. Dodgson,, and D. R. Soll,. 2005. Population genetics of ascomycetes pathogenic to humans and animals, p. 149– 188. In J. Xu (ed.), Evolutionary Genetics of Fungi. Horizon Scientific Press, Norwich, United Kingdom.

91. Pujol, C.,, J. Reynes,, F. Renaud,, M. Raymond,, M. Tibayrenc,, F. J. Ayala,, F. Janbon,, M. Mallié,, and J.-M. Bastide. 1993. The yeast Candida albicans has a clonal mode of reproduction in a population of infected human immunodeficiency virus-positive patients. Proc. Natl. Acad. Sci. USA 90: 9456– 9459.

92. Pujol, C.,, M. Pfaller,, and D. R. Soll. 2002. Ca3 fingerprinting of Candida albicans bloodstream isolates from the United States, Canada, South America, and Europe reveals a European clade. J. Clin. Microbiol. 40: 2729– 2740.

93. Pujol, C.,, S. A. Messer,, M. Pfaller,, and D. R. Soll. 2003. Drug resistance is not directly affected by mating type locus zygosity in Candida albicans. Antimicrob. Agents Chemother. 47: 1207– 1212.

94. Pujol, C.,, S. Joly,, B. Nolan,, T. Srikantha,, and D. R. Soll. 1999. Microevolutionary changes in Candida albicans identified by the complex Ca3 fingerprinting probe involve insertions and deletions of the full-length repetitive sequence RPS at specific genomic sites. Microbiology 145: 2635– 2646.

95. Pujol, C.,, S. Joly,, S. R. Lockhart,, S. Noel,, M. Tibayrenc,, and D. R. Soll. 1997. Parity among the randomly amplified polymorphic DNA method, multilocus enzyme electrophoresis, and Southern blot hybridization with the moderately repetitive DNA probe Ca3 for fingerprinting Candida albicans. J. Clin. Microbiol. 35: 2348– 2358.

96. Ramírez-Zavala, B.,, O. Reuβ,, Y.-N. Park,, K. Ohlsen,, and J. Morschhäuser. 2008. Environmental induction of white-opaque switching in Candida albicans. PLoS Pathog. 4: e1000089.

97. Ramsey, H.,, B. Morrow,, and D. R. Soll. 1994. An increase in switching frequency correlates with an increase in recombination of the ribosomal chromosomes of Candida albicans strain 3153A. Microbiology 140: 1525– 1531.

98. Rauceo, J. M.,, R. De Armond,, H. Otoo,, P. C. Kahn,, S. A. Klotz,, N. K. Gaur,, and P. N. Lipke. 2006. Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot. Cell 5: 1664– 1673.

99. Reedy, J. L.,, A. M. Floyd,, and J. Heitman. 2009. Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr. Biol. 19: 891– 899.

100. Robles, J. C.,, L. Koreen,, S. Park,, and D. S. Perlin. 2004. Multilocus sequence typing is a reliable alternative method to DNA fingerprinting for discriminating among strains of Candida albicans. J. Clin. Microbiol. 42: 2480– 2488.

101. Ruan, S.-Y.,, and P.-R. Hsueh. 2009. Invasive candidiasis: an overview from Taiwan. J. Formos. Med. Assoc. 108: 443– 451.

102. Rustad, T. R.,, D. A. Stevens,, M. A. Pfaller, and T. C. White. 2002. Homozygosity at the Candida albicans MTL locus associated with azole resistance. Microbiology 148: 1061– 1072.

103. Rustchenko, E. P.,, D. H. Howard,, and F. Sherman. 1994. Chromosomal alterations of Candida albicans are associated with the gain and loss of assimilating functions. J. Bacteriol. 176: 3231– 3241.

104. Rustchenko, E. P.,, T. M. Curran,, and F. Sherman. 1993. Variations in the number of ribosomal DNA units in morphological mutants and normal strains of Candida albicans and in normal strains of Saccharomyces cerevisiae. J. Bacteriol. 175: 7189– 7199.

105. Rustchenko-Bulgac, E. P. 1991. Variations of Candida albicans electrophoretic karyotypes. J. Bacteriol. l 73: 6586– 6596.

106. Rustchenko-Bulgac, E. P.,, F. Sherman,, and J. B. Hicks. 1990. Chromosomal rearrangements associated with morphological mutants provide a means for genetic variation in Candida albicans. J. Bacteriol. 172: 1276– 1283.

107. Sadhu, C.,, M. J. McEachern,, E. P. Rustchenko-Bulgac,, J. Schmid,, D. R. Soll,, and J. B. Hicks. 1991. Telomeric and dispersed repeat sequences in Candida yeasts and their use in strain identification. J. Bacteriol. 173: 842– 850.

108. Sahni, N.,, S. Yi,, C. Pujol,, and D. R. Sol. 2009. The white cell response to pheromone is a general characteristic of Candida albicans strains. Eukaryot. Cell 8: 251– 256.

109. Sanglard, D.,, F. Ischer,, L. Koymans,, and J. Bille. 1998. Amino acid substitutions in the cytochrome P450 lanosterol 14a-demethylase (CYP51A1) from azole-resistant Candida albicans clinical isolates contributing to the resistance to azole antifungal agents. Antimicrob. Agents Chemother. 42: 241– 253.

110. Sanz, M.,, R. Valle,, and C. Roncero. 2007. Promoter heterozygosity at the Candida albicans CHS7 gene is translated into differential expression between alleles. FEMS Yeast Res. 7: 993– 1003.

111. Scherer, S.,, and D. A. Stevens. 1988. A Candida albicans dispersed, repeated gene family and its epidemiological applications. Proc. Natl. Acad. Sci. USA 85: 1452– 1456.

112. Schmid, J.,, E. Voss,, and D. R. Soll. 1990. Computer-assisted methods for assessing strain relatedness in Candida albicans by fingerprinting with the moderately repetitive sequence Ca3. J. Clin. Microbiol. 28: 1236– 1243.

113. Selmecki, A.,, A. Forche,, and J. Berman. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367– 370.

114. Selmecki, A.,, M. Gerami-Nejad,, C. Paulson,, A. Forche,, and J. Berman. 2008. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol. Microbiol. 68: 624– 641.

115. Selmecki, A.,, S. Bergmann,, and J. Berman. 2005. Comparative genome hybridization reveals widespread aneuploidy in Candida albicans laboratory strains. Mol. Microbiol. 55: 1553– 1565.

116. Snell, R. G.,, I. F. Hermans,, R. J. Wilkins,, and B. E. Cornerl. 1987. Chromosomal variations in Candida albicans. Nucleic Acids Res. 15: 3625.

117. Slutsky, B.,, J. Buffo,, and D. R. Soll. 1985. High frequency switching of colony morphology in Candida albicans. Science 230: 666– 669.

118. Slutsky, B.,, M. Staebell,, J. Anderson,, L. Risen,, M. Pfaller,, and D. R. Soll. 1987. “White-opaque transition”: a second high-frequency switching system in Candida albicans. J. Bacteriol. 169: 189– 197.

119. Soll, D. R. 1992. High-frequency switching in Candida albicans. Clin. Microbiol. Rev. 5: 183– 203.

120. Soll, D. R. 2000. The ins and outs of DNA fingerprinting the infectious fungi. Clin. Microbiol. Rev. 13: 332– 370.

121. Soll, D. R.,, and C. Pujol. 2003. Candida albicans clades. FEMS Immunol. Med. Microbiol. 39: 1– 7.

122. Soll, D. R.,, C. J. Langtimm,, J. McDowell,, J. Hicks,, and R. Galask. 1987. High-frequency switching in Candida strains isolated from vaginitis patients. J. Clin. Microbiol. 25: 1611– 1622.

123. Soll, D. R.,, C. Pujol,, and T. Srikantha. 2009. Sex: deviant mating in yeast. Curr. Biol. 19: R509– R511.

124. Soll, D. R.,, R. Galask,, J. Schmid,, C. Hanna,, K. Mac,, and B. Morrow. 1991. Genetic dissimilarity of commensal strains carried in different anatomical locations of the same healthy women. J. Clin. Microbiol. 29: 1702– 1710.

125. Srikantha, T.,, A. R. Borneman,, K. J. Daniels,, C. Pujol,, W. Wu,, M. R. Seringhaus,, M. Gerstein,, S. Yi,, M. Snyder,, and D. R. Soll. 2006. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 5: 1674– 1687.

126. Staib, P.,, M. Kretschmar,, T. Nichterlein,, H. Hof,, and J. Morschhäuser. 2002. Host versus in vitro signals and intrastrain allelic differences in the expression of a Candida albicans virulence gene. Mol. Microbiol. 44: 1351– 1366.

127. Sudbery, P.,, N. Gow,, and J. Berman. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12: 317– 324.

128. Sullivan, D. J.,, G. P. Moran,, E. Pinjon,, A. Al-Mosaid,, C. Stokes,, C. Vaughan,, and D. C. Coleman. 2004. Comparison of the epidemiology, drug resistance mechanisms, and virulence of Candida dubliniensis and Candida albicans. FEMS Yeast Res. 4: 369– 376.

129. Suzuki, T.,, S. Nishibayashi,, T. Kuroiwa,, T. Kanbe,, and K. Tanaka. 1982. Variance of ploidy in Candida albicans. J. Bacteriol. 152: 893– 896.

130. Tavanti, A.,, A. D. Davidson,, M. J. Fordyce,, N. A. Gow,, M. C. Maiden,, and F. C. Odds. 2005. Population structure and properties of Candida albicans, as determined by multilocus sequence typing. J. Clin. Microbiol. 43: 5601– 5613.

131. Tavanti, A.,, N. A. R. Gow,, M. C. J. Maiden,, F. C. Odds,, and D. J. Shaw. 2004. Genetic evidence for recombination in Candida albicans based on haplotype analysis. Fungal Genet. Biol. 41: 553– 562.

132. Tsong, A. E.,, M. G. Miller,, R. M. Raisner,, and A. D. Johnson. 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115: 389– 399.

133. Tzung, K. W.,, R. M. Williams,, S. Scherer,, N. Federspiel,, T. Jones,, N. Hansen,, V. Bivolarevic,, L. Huizar,, C. Komp,, R. Surzycki,, R. Tamse,, R. W. Davis,, and N. Agabian. 2001. Genomic evidence for a complete sexual cycle in Candida albicans. Proc. Natl. Acad. Sci. USA 98: 3249– 3253.

134. Uhl, M. A.,, M. Biery,, N. Craig,, and A. D. Johnson. 2003. Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 22: 2668– 2678.

135. Van Kruiningen, H. J.,, M. Joossens,, S. Vermeire,, S. Joossens,, S. Debeugny,, C. Gower-Rousseau,, A. Cortot,, J. F. Colombel,, P. Rutgeerts,, and R. Vlietinck. 2005. Environmental factors in familial Crohn’s disease in Belgium. Inflamm. Bowel Dis. 11: 360– 365.

136. Welch, D. M.,, and M. Meselson. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211– 1215.

137. Wellington, M.,, and E. Rustchenko. 2005. 5-Fluoro-orotic acid induces chromosome alterations in Candida albicans. Yeast 22: 57– 70.

138. Whelan, W. L.,, and D. R. Soll. 1982. Mitotic recombination in Candida albicans: recessive lethal alleles linked to a gene required for methionine biosynthesis. Mol. Gen. Genet. 187: 477– 485.

139. White, T. C. 1997. The presence of an R467K amino acid substitution and loss of allelic variation correlate with an azole-resistant lanosterol 14-alpha-demethylase in Candida albicans. Antimicrob. Agents Chemother. 41: 1488– 1494.

140. White, T. C.,, K. A. Marr,, and R. A. Bowden. 1998. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev. 11: 382– 402.

141. Wickes, B.,, J. Staudinger,, B. B. Magee,, K.-J. Kwon-Chung,, P. T. Magee,, and S. Scherer. 1991 Physical and genetic mapping of Candida albicans: several genes previously assigned to chromosome 1 map to chromosome R, the rDNA-containing linkage group. Infect. Immun. 59: 2480– 2484.

142. Wilson, M. J.,, D. W. Williams,, M. D. L. Forbes,, I. G. Finlay,, and M. A. O. Lewis. 2001. A molecular epidemiological study of sequential oral isolates of Candida albicans from terminally ill patients. J. Oral Pathol. Med. 30: 206– 212.

143. Wu, W.,, C. Pujol,, S. R. Lockhart,, and D. R. Soll. 2005. Chromosome loss followed by duplication is the major mechanism of spontaneous mating-type locus homozygosis in Candida albicans. Genetics 169: 1311– 1327.

144. Wu, W.,, S. R. Lockhart,, C. Pujol,, T. Srikantha,, and D. R. Soll. 2007. Heterozygosity of genes on the sex chromosome regulates Candida albicans virulence. Mol. Microbiol. 64: 1587– 1604.

145. Yi, S.,, N. Sahni,, K. J. Daniels,, C. Pujol,, T. Srikantha,, and D. R. Soll. 2008. The same receptor, G protein, and mitogen-activated protein kinase pathway activate different downstream regulators in the alternative white and opaque pheromone responses of Candida albicans. Mol. Biol. Cell 19: 957– 970.

146. Yi, S.,, N. Sahni,, C. Pujol,, K. J. Daniels,, T. Srikantha,, N. Ma,, and D. R. Soll. 2009. A Candida albicans-specific region of the a-pheromone receptor plays a selective role in the white cell pheromone response. Mol. Microbiol. 71: 925– 947.

147. Zeyl, C., 2007. Ploidy and the sexual yeast genome in theory, nature, and experiment, p. 507– 525. In J. Heitman,, J. W. Kronstad,, J. W. Taylor,, and L. A. Casselton (ed.), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC.

148. Zhao, X.,, C. Pujol,, D. R. Soll,, and L. L. Hoyer. 2003. Allelic variation in the contiguous loci encoding Candida albicans ALS5, ALS1 and ALS9. Microbiology 149: 2947– 2960.

149. Zhao, X.,, S.-H. Oh,, and L. L. Hoyer. 2007. Unequal contribution of ALS9 alleles to adhesion between Candida albicans and human vascular endothelial cells. Microbiology 153: 2342– 2350.

150. Zordan, R. E.,, D. J. Galgoczy,, and A. D. Johnson. 2006. Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc. Natl. Acad. Sci. USA 103: 12807– 12812.

Tables

Genome Plasticity in Candida albicans

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817213.chap18-1,webId=/content/author/10.1128/9781555817213.chap18-1,properties={foaf_givenname=Claude, foaf_name=Claude Pujol, foaf_surname=Pujol, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817213.chap18-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817213.chap18-2,webId=/content/author/10.1128/9781555817213.chap18-2,properties={foaf_givenname=David R., foaf_name=David R. Soll, foaf_surname=Soll, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817213.chap18-aff2]]}]]

/content/10.1128/9781555817213.chap18.tab18-1

TABLE 1

The proportion of C. albicans MTL-homozygous strains increases in older collections a

10.1128/9781555817213/tab18-1_thmb.gif

10.1128/9781555817213/tab18-1.gif

TABLE 1

The proportion of C. albicans MTL-homozygous strains increases in older collections a