Phenotypic consequences of a spontaneous loss of heterozygosity in a common laboratory strain of Candida albicans

Genetics

Volumn 203, Issue 3, 2016, Pages 1161-1176

  Ciudad, Toni ^a   Hickman, Meleah ^b   Bellido, Alberto ^a   Berman, Judith ^b,c   Larriba, Germán ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b UNIVERSITY OF MINNESOTA   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Candida albicans; Growth polarization; LOH; MBP1; MMS susceptibility

Indexed keywords

FUNGAL PROTEIN; MBP1 PROTEIN; MESYLIC ACID METHYL ESTER; ORF19.5854.1 PROTEIN; POL1 PROTEIN; SNF5 PROTEIN; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT;

ALLELE; ARTICLE; CANDIDA ALBICANS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE DISRUPTION; GENETIC SUSCEPTIBILITY; HETEROZYGOSITY LOSS; HOMOZYGOSITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; BIOSYNTHESIS; DNA DAMAGE; DNA REPAIR; DRUG EFFECTS; EPISTASIS; GENE EXPRESSION REGULATION; GENETICS;

ALLELES; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; COMPARATIVE GENOMIC HYBRIDIZATION; DNA DAMAGE; DNA REPAIR; EPISTASIS, GENETIC; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; LOSS OF HETEROZYGOSITY; METHYL METHANESULFONATE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84979911704     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.189274     Document Type: Article

References (77)

1. Abbey, D., M. Hickman, D. Gresham, and J. Berman, 2011 Highresolution SNP/CGH microarrays reveal the accumulation of loss of heterozygosity in commonly used Candida albicans strains. G3 (Bethesda) 1: 523–530.
2. Alonso-Monge, R., F. Navarro-García, E. Román, A. I. Negredo, B. Eisman et al., 2003 The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot. Cell 2: 351–361.
3. Andaluz, E., J. J. Coque, R. Cueva, and G. Larriba, 2001 Sequencing of a 4.3 kbp region of chromosome 2 of Candida albicans reveals the presence of homologues of SHE9 from Saccharomyces cerevisiae and of bacterial phosphatidylinositol-phospholipase C. Yeast 18: 711–721.
4. Andaluz, E., A. Bellido, J. Gómez-Raja, A. Selmecki, K. Bouchonville et al., 2011 Rad52 function prevents chromosome loss and truncation in Candida albicans. Mol. Microbiol. 79: 1462–1482.
5. Aramayo, R., and R. L. Metzenberg, 1996 Meiotic transvection in fungi. Cell 86: 103–113.
6. Arbour, M., E. Epp, H. Hogues, A. Sellam, C. Lacroix et al., 2009 Widespread occurrence of chromosomal aneuploidy following the routine production of Candida albicans mutants. FEMS Yeast Res. 9: 1070–1077.
7. Bain, J. M., C. Stubberfield, and N. A. Gow, 2001 Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol. Lett. 204: 323–328.
8. Barnes, G., and D. Rio, 1997 DNA double-strand-break sensitivity, DNA replication, and cell cycle arrest phenotypes of Ku-deficient Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94: 867– 872.
9. Begley, T. J., A. S. Rosenbach, T. Ideker, and L. D. Samson, 2002 Damage recovery pathways in Saccharomyces cerevisiae revealed by genomic phenotyping and interactome mapping. Mol. Cancer Res. 1: 103–112.
10. Begley, T. J., A. S. Rosenbach, T. Ideker, and L. D. Samson, 2004 Hot spots for modulating toxicity identified by genomic phenotyping and localization mapping. Mol. Cell 16: 117–125.
11. Boiteux, S., and S. Jinks-Robertson, 2013 DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics 193: 1025–1064.
12. Bouchonville, K., A. Forche, K. E. Tang, A. Selmecki, and J. Berman, 2009 Aneuploid chromosomes are highly unstable during DNA transformation of Candida albicans. Eukaryot. Cell 8: 1554–1566.
13. Brand, A., D. M. MacCallum, A. J. Brown, N. A. Gow, and F. C. Odds, 2004 Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3: 900–909.
14. Braun, B. R., M. van Het Hoog, C. d’Enfert, M. Martchenko, J. Dungan et al., 2005 A human-curated annotation of the Candida albicans genome. PLoS Genet. 1: 36–57.
15. Butler, G., M. D. Rasmussen, M. F. Lin, M. A. Santos, S. Sakthikumar et al., 2009 Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657–662.
16. Chai, B., J. Huang, B. R. Cairns, and B. C. Laurent, 2005 Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19: 1656–1661.
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. Chico, L., T. Ciudad, M. Hsu, N. F. Lue, and G. Larriba, 2011 The Candida albicans Ku70 modulates telomere length and structure by regulating both telomerase and recombination. PLoS One 6: e23732.
19. Coletta, A., J. W. Pinney, D. Y. Solís, J. Marsh, S. R. Pettifer et al., 2010 Low-complexity regions within protein sequences have position-dependent roles. BMC Syst. Biol. 4: 43.
20. Critchlow, S. E., and S. P. Jackson, 1998 DNA end-joining: from yeast to man. Trends Biochem. Sci. 23: 394–398.
21. Daley, J. M., P. L. Palmbos, D. Wu, and T. E. Wilson, 2005 Nonhomologous end joining in yeast. Annu. Rev. Genet. 39: 431–451.
22. Deem, A., A. Keszthelyi, T. Blackgrove, A. Vayl, B. Coffey et al., 2011 Break-induced replication is highly inaccurate. PLoS Biol. 9: e1000594.
23. Fan, H. Y., K. K. Cheng, and H. L. Klein, 1996 Mutations in the RNA polymerase II transcription machinery suppress the hyperrecombination mutant hpr1 delta of Saccharomyces cerevisiae. Genetics 142: 749–759.
24. Finkel, J. S., W. Xu, D. Huang, E. M. Hill, J. V. Desai et al., 2012 Portrait of Candida albicans adherence regulators. PLoS Pathog. 8: e1002525.
25. Fonzi, W. A., and M. Y. Irwin, 1993 Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717–728.
26. Forche, A., K. Alby, D. Schaefer, A. D. Johnson, J. Berman et al., 2008 The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 6: e110.
27. Forche, A., M. Steinbach, and J. Berman, 2009a Efficient and rapid identification of Candida albicans allelic status using SNP-RFLP. FEMS Yeast Res. 9: 1061–1069.
28. Forche, A., P. T. Magee, A. Selmecki, J. Berman, and G. May, 2009b Evolution in Candida albicans populations during a single passage through a mouse host. Genetics 182: 799–811.
29. Forche, A., D. Abbey, T. Pisithkul, M. A. Weinzierl, T. Ringstrom et al., 2011 Stress alters rates and types of loss of heterozygosity in Candida albicans. MBio 2: e00129–e11.
30. Ford, C. B., J. M. Funt, D. Abbey, L. Issi, C. Guiducci et al., 2015 The evolution of drug resistance in clinical isolates of Candida albicans. eLife 4: e00662.
31. Foster, S. S., A. Balestrini, and J. H. Petrini, 2011 Functional interplay of the Mre11 nuclease and Ku in the response to replication-associated DNA damage. Mol. Cell. Biol. 31: 4379–4389.
32. Gerstein, A. C., and J. Berman, 2015 Shift and adapt: the costs and benefits of karyotype variations. Curr. Opin. Microbiol. 26: 130–136.
33. Gómez-Raja, J., E. Andaluz, B. Magee, R. Calderone, and G. Larriba, 2008 A single SNP, G929T (Gly310Val), determines the presence of a functional and a non-functional allele of HIS4 in Candida albicans SC5314: detection of the non-functional allele in laboratory strains. Fungal Genet. Biol. 45: 527–541.
34. Hicks, W. M., M. Kim, and J. E. Haber, 2010 Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329: 82–85.
35. Horton, J. K., and S. H. Wilson, 2007 Hypersensitivity phenotypes associated with genetic and synthetic inhibitor-induced base excision repair deficiency. DNA Repair (Amst.) 6: 530–543.
36. Hussein, B., H. Huang, A. Glory, A. Osmani, S. Kaminskyj et al., 2011 G1/S transcription factor orthologues Swi4p and Swi6p are important but not essential for cell proliferation and influence hyphal development in the fungal pathogen Candida albicans. Eukaryot. Cell 10: 384–397.
37. Jones, T., N. A. Federspiel, H. Chibana, J. Dungan, S. Kalman et al., 2004 The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 101: 7329–7334.
38. Larriba, G., and R. Calderone, 2008 Heterozygosity and loss of heterozygosity in Candida albicans, Pathogenic Fungi. Insights in Molecular Biology, edited by G. San Blas, and G. Calderone. Caister Academic Press, Norfolk, UK.
39. Lay, J., L. K. Henry, J. Clifford, Y. Koltin, C. E. Bulawa et al., 1998 Altered expression of selectable marker URA3 in genedisrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66: 5301–5306.
40. Lee, P. S., and T. D. Petes, 2010 From the cover: mitotic gene conversion events induced in G1-synchronized yeast cells by gamma rays are similar to spontaneous conversion events. Proc. Natl. Acad. Sci. USA 107: 7383–7388.
41. Lee, P. S., P. W. Greenwell, M. Dominska, M. Gawel., M. Hamilton et al., 2009 A fine-structure map of spontaneous mitotic crossovers in the yeast Saccharomyces cerevisiae. PLoS Genet. 5: e1000410.
42. Lephart, P. R., and P. T. Magee, 2006 Effect of the major repeat sequence on mitotic recombination in Candida albicans. Genetics 174: 1737–1744.
43. Loll-Krippleber, R., C. d’Enfert, A. Feri, D. Diogo, A. Perin et al., 2014 A study of the DNA damage checkpoint in Candida albicans: uncoupling of the functions of Rad53 in DNA repair, cell cycle regulation and genotoxic stress-induced polarized growth. Mol. Microbiol. 91: 452–471.
44. Magee, B. B., and P. T. Magee, 2000 Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289: 310–313.
45. Mandegar, M. A., and S. P. Otto, 2007 Mitotic recombination counteracts the benefits of genetic segregation. Proc. Biol. Sci. 274: 1301–1307.
46. Messerschmitt, M., S. Jakobs, F. Vogel, S. Fritz, K. S. Dimmer et al., 2003 The inner membrane protein Mdm33 controls mitochondrial morphology in yeast. J. Cell Biol. 160: 553–564.
47. Muzzey, D., K. Schwartz, J. S. Weissman, and G. Sherlock, 2013 Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure. Genome Biol. 14: R97.
48. Muzzey, D., G. Sherlock, and J. S. Weissman, 2014 Extensive and coordinated control of allele-specific expression by both transcription and translation in Candida albicans. Genome Res. 24: 963–973.
49. Nalls, M. A., R. J. Guerreiro, J. Simon-Sanchez, J. T. Bras, B. J. Traynor et al., 2009 Extended tracts of homozygosity identify novel candidate genes associated with late-onset Alzheimer’s disease. Neurogenetics 10: 183–190.
50. Niimi, K., B. C. Monk, A. Hirai, K. Hatakenaka, T. Umeyama et al., 2010 Clinically significant micafungin resistance in Candida albicans involves modification of a glucan synthase catalytic subunit GSC1 (FKS1) allele followed by loss of heterozygosity. J. Antimicrob. Chemother. 65: 842–852.
51. Noble, S. M., and A. D. Johnson, 2005 Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4: 298–309.
52. Noble, S. M., S. French, L. A. Kohn, V. Chen, and A. D. Johnson, 2010 Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42: 590–598.
53. Otto, S. P., and A. C. Gerstein, 2008 The evolution of haploidy and diploidy. Curr. Biol. 18: R1121–R1124.
54. Oum, J. H., C. Seong, Y. Kwon, J. H. Ji, A. Sid et al., 2011 RSC facilitates Rad59-dependent homologous recombination between sister chromatids by promoting cohesin loading at DNA double-strand breaks. Mol. Cell. Biol. 31: 3924–3937.
55. Park, Y. N., and J. Morschhäuser, 2005 Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 4: 1328–1342.
56. Poulter, R., 1990 Classical methods for the genetic analysis of Candida albicans, pp. 75–121 in The Genetics of Candida, Chapter 3. CRC Press, Boca Raton, FL.
57. Reuss, O., A. Vik, R. Kolter, and J. Morschhäuser, 2004 The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119–127.
58. Rustchenko, E., 2007 Chromosome instability in Candida albicans. FEMS Yeast Res. 7: 2–11.
59. Sasse, C., N. Dunkel, T. Schäfer, S. Schneider, F. Dierolf et al., 2012 The stepwise acquisition of fluconazole resistance mutations causes a gradual loss of fitness in Candida albicans. Mol. Microbiol. 86: 539–556.
60. Schoustra, S. E., A. J. Debets, M. Slakhorst, and R. F. Hoekstra, 2007 Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLoS Genet. 3: e68.
61. Selmecki, A., S. Bergmann, and J. Berman, 2005 Comparative genome hybridization reveals widespread aneuploidy in Candida albicans laboratory strains. Mol. Microbiol. 55: 1553–1565.
62. Selmecki, A., A. Forche, and J. Berman, 2006 Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367–370.
63. 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.
64. Sharkey, L. L., W. L. Liao, A. K. Ghosh, and W. A. Fonzi, 2005 Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151: 1061–1071.
65. Shi, Q. M., Y. M. Wang, X. D. Zheng, R. T. Lee, and Y. Wang, 2007 Critical role of DNA checkpoints in mediating genotoxic-stress-induced filamentous growth in Candida albicans. Mol. Biol. Cell 18: 815–826.
66. Sousa, C. A., S. Hanselaer, and E. V. Soares, 2015 ABCC subfamily vacuolar transporters are involved in Pb (lead) detoxification in Saccharomyces cerevisiae. Appl. Biochem. Biotechnol. 175: 65– 74.
67. St Charles, J., E. Hazkani-Covo, Y. Yin, S. L. Andersen, F. S. Dietrich et al., 2012 High-resolution genome-wide analysis of irradiated (UV and ɤ-rays) diploid yeast cells reveals a high frequency of genomic loss of heterozygosity (LOH) events. Genetics 190: 1267–1284.
68. Staib, P., M. Kretschmar, T. Nichterlein, H. Hof, and J. Morschhäuser, 2002 Host vs. in vitro signals and intrastrain allelic differences in the expression of a Candida albicans virulence gene. Mol. Microbiol. 44: 1351–1366.
69. Sun, L. L., W. J. Li, H. T. Wang, J. Chen, P. Deng et al., 2011 Protein phosphatase Pph3 and its regulatory subunit Psy2 regulate Rad53 dephosphorylation and cell morphogenesis during recovery from DNA damage in Candida albicans. Eukaryot. Cell 10: 1565–1573.
70. Symington, L. S., R. Rothstein, and M. Lisby, 2014 Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198: 795–835.
71. Travesa, A., D. Kuo, R. A. de Bruin, T. I. Kalashnikova, M. Guaderrama et al., 2012 DNA replication stress differentially regulates G1/S genes via Rad53-dependent inactivation of Nrm1. EMBO J. 31: 1811–1822.
72. van het Hoog, M., T. J. Rast, M. Martchenko, S. Grindle, D. Dignard et al., 2007 Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol. 8: R52.
73. Wang, H., J. Gao, W. Li, A. H. Wong, K. Hu et al., 2012 Pph3 dephosphorylation of Rad53 is required for cell recovery from MMS-induced DNA damage in Candida albicans. PLoS One 7: e37246.
74. Weinreich, D. M., R. A. Watson, and L. Chao, 2005 Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59: 1165–1174.
75. Wellington, M., and E. Rustchenko, 2005 5-Fluoro-orotic acid induces chromosome alterations in Candida albicans. Yeast 22: 57–70.
76. Wilson, R. B., D. Davis, and A. P. Mitchell, 1999 Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181: 1868–1874.
77. Yang, T. L., Y. Guo, L. S. Zhang, Q. Tian, H. Yan et al., 2010 Runs of homozygosity identify a recessive locus 12q21.31 for human adult height. J. Clin. Endocrinol. Metab. 95: 3777–3782.