Parasex Generates Phenotypic Diversity de Novo and Impacts Drug Resistance and Virulence in Candida albicans
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Abstract Candida albicans is a diploid fungus that is a frequent cause of mucosal and systemic infections in humans. This species exhibits an unusual parasexual cycle in which mating produces tetraploid cells that undergo a nonmeiotic program of concerted chromosome loss to return to a diploid or aneuploid state. In this work, we used a multipronged approach to examine the capacity of parasex to generate diversity in C. albicans. First, we compared the phenotypic properties of 32 genotyped progeny and observed wide-ranging differences in fitness, filamentation, biofilm formation, and virulence. Strikingly, one parasexual isolate displayed increased virulence relative to parental strains using a Galleria mellonella model of infection, establishing that parasex has the potential to enhance pathogenic traits. Next, we examined parasexual progeny derived from homothallic, same-sex mating events, and reveal that parasex can generate diversity de novo from identical parental strains. Finally, we generated pools of parasexual progeny and examined resistance of these pools to environmental stresses. Parasexual progeny were generally less fit than control strains across most test conditions, but showed an increased ability to grow in the presence of the antifungal drug fluconazole (FL). FL-resistant progeny were aneuploid isolates, often being diploid strains trisomic for both Chr3 and Chr6. Passaging of these aneuploid strains frequently led to loss of the supernumerary chromosomes and a concomitant decrease in drug resistance. These experiments establish that parasex generates extensive phenotypic diversity de novo, and that this process has important consequences for both virulence and drug resistance in C. albicans populations.
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Elevated copy numbers of chromosomes 3 and 6 are associated with fluconazole resistance in C. albicans.
“Another recent study added elevated copy numbers of chromosomes 3 and 6 to the list of genome rearrangements associated with fluconazole resistance in C. albicans [83].”
From Evolutionary Emergence of Drug Resistance in Candida Opportunistic Pathogens (2018) · cites this paper as [83]
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Cites
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437 · see citing works
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390 · see citing works
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
Thorvaldsdottir, H., Robinson, J. T., & Mesirov, J. P. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbs017 · Cited by 9,049 · see citing works
Walker, B. J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C. A., Zeng, Q., Wortman, J. R., Young, S., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112963 · Cited by 8,994 · see citing works
Van der Auwera, G. A., Carneiro, M. O., Hartl, C., Poplin, R., del Angel, G., Levy‐Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., et al. (2013) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1110s43 · Cited by 6,687 · see citing works
Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P., & Edmond, M. B. (2004) · Clinical Infectious Diseases · doi:10.1086/421946 · Cited by 4,496 · see citing works
Guide to Yeast Genetics and Molecular Biology
Kurtzman, C. P., Guthrie, C., & Fink, G. R. (1993) · Mycologia · doi:10.2307/3760517 · Cited by 2,363 · see citing works
<i>Candida albicans</i> pathogenicity mechanisms
Mayer, F. L., Wilson, D., & Hube, B. (2013) · Virulence · doi:10.4161/viru.22913 · Cited by 1,848 · see citing works
Virulence factors of Candida albicans
Calderone, R. A., & Fonzi, W. A. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02094-7 · Cited by 1,331 · see citing works
Attributable Mortality of Nosocomial Candidemia, Revisited
Gudlaugsson, O., Gillespie, S., Lee, K., Berg, J. V., Hu, J., Messer, S., Herwaldt, L., Pfaller, M., & Diekema, D. (2003) · Clinical Infectious Diseases · doi:10.1086/378745 · Cited by 1,140 · see citing works
Growth of Candida albicans hyphae
Sudbery, P. E. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2636 · Cited by 1,110 · see citing works
Evolution of pathogenicity and sexual reproduction in eight Candida genomes
Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A. S., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., et al. (2009) · Nature · doi:10.1038/nature08064 · Cited by 1,065 · see citing works
<i>Candida albicans</i> Biofilms and Human Disease
Nobile, C. J., & Johnson, A. D. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104330 · Cited by 1,057 · see citing works
Molecular Evidence for the Early Colonization of Land by Fungi and Plants
Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., & Hedges, S. B. (2001) · Science · doi:10.1126/science.1061457 · Cited by 1,020 · see citing works
Guide to yeast genetics and molecular biology
Simanis, V. (1992) · Trends in Cell Biology · doi:10.1016/0962-8924(92)90020-n · Cited by 1,003 · see citing works
The diploid genome sequence of Candida albicans
Jones, T., Federspiel, N. A., Chibana, H., Dungan, J. M., Kalman, S., Magee, B. B., Newport, G., Thorstenson, Y. R., Agabian, N. M., Magee, P. T., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401648101 · Cited by 768 · see citing works
Aneuploidy and Isochromosome Formation in Drug-Resistant <i>Candida albicans</i>
Selmecki, A., Forche, A., & Berman, J. (2006) · Science · doi:10.1126/science.1128242 · Cited by 733 · see citing works
A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
Nobile, C. J., Fox, E. P., Nett, J. E., Sorrells, T. R., Mitrovich, Q. M., Hernday, A. D., Tuch, B. B., Andes, D. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2011.10.048 · Cited by 711 · see citing works
Noble, S. M., French, S., Kohn, L. A., Chen, V., & Johnson, A. D. (2010) · Nature Genetics · doi:10.1038/ng.605 · Cited by 678 · see citing works
Saville, S. P., Lazzell, A. L., Monteagudo, C., & Lopez-Ribot, J. L. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.1053-1060.2003 · Cited by 655 · see citing works
Guide to Yeast Genetics and Molecular Biology
(1991) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(00)x0276-5 · Cited by 644 · see citing works
Genetic control of Candida albicans biofilm development
Finkel, J. S., & Mitchell, A. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2475 · Cited by 613 · see citing works
Sanglard, D., Ischer, F., Monod, M., & Bille, J. (1997) · Microbiology · doi:10.1099/00221287-143-2-405 · Cited by 587 · see citing works
Miller, M. G., & Johnson, A. D. (2002) · Cell · doi:10.1016/s0092-8674(02)00837-1 · Cited by 569 · see citing works
Short- and long-term effects of chromosome mis-segregation and aneuploidy
Santaguida, S., & Amon, A. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4025 · Cited by 535 · see citing works
Prasad, R., De Wergifosse, P., Goffeau, A., & Balzi, E. (1995) · Current Genetics · doi:10.1007/bf00352101 · Cited by 486 · see citing works
Evidence for Mating of the "Asexual" Yeast Candida albicans in a Mammalian Host
Hull, C. M., Raisner, R. M., & Johnson, A. D. (2000) · Science · doi:10.1126/science.289.5477.307 · Cited by 464 · see citing works
Sex increases the efficacy of natural selection in experimental yeast populations
Goddard, M. R., Godfray, H. C. J., & Burt, A. (2005) · Nature · doi:10.1038/nature03405 · Cited by 464 · see citing works
Guide to yeast genetics and molecular biology
Guthrie, C. 1., & Fink, G. R. 1. (n.d.) · Cited by 449 · see citing works
Induction of Mating in Candida albicans by Construction of MTL a and MTL α Strains
Magee, B. B., & Magee, P. T. (2000) · Science · doi:10.1126/science.289.5477.310 · Cited by 443 · see citing works
Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex
Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish, R. C., & Lively, C. M. (2011) · Science · doi:10.1126/science.1206360 · Cited by 434 · see citing works
Sex speeds adaptation by altering the dynamics of molecular evolution
McDonald, M. J., Rice, D. P., & Desai, M. M. (2016) · Nature · doi:10.1038/nature17143 · Cited by 425 · see citing works
Dating divergences in the Fungal Tree of Life: review and new analyses
Taylor, J. W., & Berbee, M. L. (2006) · Mycologia · doi:10.3852/mycologia.98.6.838 · Cited by 424 · see citing works
Coste, A., Turner, V., Ischer, F., Morschhäuser, J., Forche, A., Selmecki, A., Berman, J., Bille, J., & Sanglard, D. (2006) · Genetics · doi:10.1534/genetics.105.054767 · Cited by 385 · see citing works
PERSPECTIVE: SEX, RECOMBINATION, AND THE EFFICACY OF SELECTION?WAS WEISMANN RIGHT?
Burt, A. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00038.x · Cited by 382 · see citing works
Chromosomal duplication is a transient evolutionary solution to stress
Yona, A. H., Manor, Y. S., Herbst, R. H., Romano, G. H., Mitchell, A., Kupiec, M., Pilpel, Y., & Dahan, O. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211150109 · Cited by 376 · see citing works
Identification of Aneuploidy-Tolerating Mutations
Torres, E. M., Dephoure, N., Panneerselvam, A., Tucker, C. M., Whittaker, C. A., Gygi, S. P., Dunham, M. J., & Amon, A. (2010) · Cell · doi:10.1016/j.cell.2010.08.038 · Cited by 371 · see citing works
Sporulation in the Budding Yeast Saccharomyces cerevisiae
Neiman, A. M. (2011) · Genetics · doi:10.1534/genetics.111.127126 · Cited by 368 · see citing works
Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae
Brennan, M., Thomas, D. Y., Whiteway, M. S., & Kavanagh, K. A. (2002) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2002.tb00617.x · Cited by 360 · see citing works
Morschhäuser, J., Barker, K. S., Liu, T. T., Blaß-Warmuth, J., Homayouni, R., & Rogers, P. D. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030164 · Cited by 355 · see citing works
Ni, M., Feretzaki, M., Sun, S., Wang, X., & Heitman, J. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132536 · Cited by 352 · see citing works
The evolution of drug resistance in clinical isolates of Candida albicans.
Ford, C. B., Funt, J. M., Abbey, D., Issi, L., Guiducci, C., Martinez, D. A., Delorey, T., Li, B. Y., White, T. C., Cuomo, C., et al. (2015) · eLife · doi:10.7554/elife.00662 · Cited by 348 · see citing works
Bennett, R. J., & Johnson, A. D. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg235 · Cited by 343 · see citing works
Self-citationForche, A., Alby, K., Schaefer, D., Johnson, A. D., Berman, J., & Bennett, R. J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060110 · Cited by 338 · see citing works
Self-citationRancati, G. I., Pavelka, N., Fleharty, B., Noll, A. C., Trimble, R., Walton, K., Perera, A. G., Staehling‐Hampton, K., Seidel, C. W., & Li, R. (2008) · Cell · doi:10.1016/j.cell.2008.09.039 · Cited by 335 · see citing works
Selmecki, A., Gerami‐Nejad, M., Paulson, C., Forche, A., & Berman, J. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06176.x · Cited by 325 · see citing works
Genetic and phenotypic intra-species variation in <i>Candida albicans</i>
Hirakawa, M. P., Martinez, D. A., Sakthikumar, S., Anderson, M. Z., Berlin, A., Gujja, S., Zeng, Q., Zisson, E., Wang, J. M., Greenberg, J. M., et al. (2015) · Genome Research · doi:10.1101/gr.174623.114 · Cited by 320 · see citing works
Self-citationSelmecki, A. M., Dulmage, K., Cowen, L. E., Anderson, J. B., & Berman, J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000705 · Cited by 319 · see citing works
Lehtonen, J., Jennions, M. D., & Kokko, H. (2011) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2011.09.016 · Cited by 312 · see citing works
Methods for usingGalleria mellonellaas a model host to study fungal pathogenesis
Fuchs, B. B., O’Brien, E., Khoury, J. B. E., & Mylonakis, E. E. (2010) · Virulence · doi:10.4161/viru.1.6.12985 · Cited by 310 · see citing works
Molecular Phylogenetics of Candida albicans
Odds, F. C., Bougnoux, M., Shaw, D. J., Bain, J. M., Davidson, A. D., Diogo, D., Jacobsen, M. D., Lecomte, M., Li, S.-Y., Tavanti, A., et al. (2007) · Eukaryotic Cell · doi:10.1128/ec.00041-07 · Cited by 306 · see citing works
The ‘obligate diploid’ Candida albicans forms mating-competent haploids
Hickman, M. A., Zeng, G., Forche, A., Hirakawa, M. P., Abbey, D., Harrison, B. D., Wang, Y.-M., Su, C.-H., Bennett, R. J., Wang, Y., et al. (2013) · Nature · doi:10.1038/nature11865 · Cited by 284 · see citing works
Self-citationDunkel, N., Blaß, J., Rogers, P. D., & Morschhäuser, J. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06309.x · Cited by 278 · see citing works
Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy
Chen, G., Bradford, W. D., Seidel, C. W., & Li, R. (2012) · Nature · doi:10.1038/nature10795 · Cited by 274 · see citing works
Jokela, J., Dybdahl, M. F., & Lively, C. M. (2009) · The American Naturalist · doi:10.1086/599080 · Cited by 252 · see citing works
Genomic Plasticity of the Human Fungal Pathogen Candida albicans
Selmecki, A., Forche, A., & Berman, J. (2010) · Eukaryotic Cell · doi:10.1128/ec.00060-10 · Cited by 247 · see citing works
Development of an insect model for the in vivo pathogenicity testing of yeasts
Cotter, G., Doyle, S., & Kavanagh, K. A. (2000) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2000.tb01427.x · Cited by 234 · see citing works
Mate and fuse: how yeast cells do it
Merlini, L., Dudin, O., & Martin, S. G. (2013) · Open Biology · doi:10.1098/rsob.130008 · Cited by 228 · see citing works
Gräser, Y., Volovsek, M., Arrington, J., Schönian, G., Presber, W., Mitchell, T. G., & Vilgalys, R. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.22.12473 · Cited by 222 · see citing works
Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans
Alby, K., Schaefer, D., & Bennett, R. J. (2009) · Nature · doi:10.1038/nature08252 · Cited by 218 · see citing works
Self-citationMycobiota in gastrointestinal diseases
Mukherjee, P. K., Sendid, B., Hoarau, G., Colombel, J., Poulain, D., & Ghannoum, M. A. (2014) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2014.188 · Cited by 211 · see citing works
The Flo8 Transcription Factor Is Essential for Hyphal Development and Virulence in Candida albicans
Cao, F., Lane, S., Raniga, P. P., Lü, Y., Zhou, Z., Ramon, K., Chen, J., & Liu, H. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0502 · Cited by 207 · see citing works
PERSPECTIVE: SEX, RECOMBINATION, AND THE EFFICACY OF SELECTION—WAS WEISMANN RIGHT?
Burt, A. (2000) · Evolution · doi:10.1554/0014-3820(2000)054[0337:psrate]2.0.co;2 · Cited by 181 · see citing works
A Tetraploid Intermediate Precedes Aneuploid Formation in Yeasts Exposed to Fluconazole
Harrison, B. D., Hashemi, J., Bibi, M., Pulver, R., Bavli, D., Nahmias, Y., Wellington, M., Sapiro, G., & Berman, J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001815 · Cited by 174 · see citing works
Fox, E. P., Bui, C. K., Nett, J. E., Hartooni, N., Mui, M. C., Andes, D. R., Nobile, C. J., & Johnson, A. D. (2015) · Molecular Microbiology · doi:10.1111/mmi.13002 · Cited by 173 · see citing works
A Review of Red Queen Models for the Persistence of Obligate Sexual Reproduction
Lively, C. M. (2010) · Journal of Heredity · doi:10.1093/jhered/esq010 · Cited by 168 · see citing works
Identification and Characterization of a Candida albicans Mating Pheromone
Bennett, R. J., Uhl, M., Miller, M. G., & Johnson, A. D. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.22.8189-8201.2003 · Cited by 166 · see citing works
Self-citationAssembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes
Hoog, M. V. H., Rast, T. J., Martchenko, M., Grindle, S. M., Dignard, D., Hogues, H., Cuomo, C. A., Berriman, M., Scherer, S., Magee, B. B., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r52 · Cited by 166 · see citing works
Wirsching, S., Michel, S., & Morschhäuser, J. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01899.x · Cited by 158 · see citing works
Evolution of Eukaryotic Microbial Pathogens via Covert Sexual Reproduction
Heitman, J. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.06.011 · Cited by 155 · see citing works
Ni, M., Feretzaki, M., Li, W., Averette, A. F., Mieczkowski, P. A., Dietrich, F. S., & Heitman, J. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001653 · Cited by 155 · see citing works
Fungal mating pheromones: Choreographing the dating game
Jones, S. K., & Bennett, R. J. (2011) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2011.04.001 · Cited by 150 · see citing works
Self-citationProperty Differences among the Four Major Candida albicans Strain Clades
MacCallum, D. M., Castillo, L., Nather, K., Munro, C. A., Brown, A. J. P., Gow, N. A. R., & Odds, F. C. (2009) · Eukaryotic Cell · doi:10.1128/ec.00387-08 · Cited by 150 · see citing works
Specific Chromosome Alterations in Fluconazole-Resistant Mutants of Candida albicans
Perepnikhatka, V. I., Fischer, F. J., Niimi, M., Baker, R. A., Cannon, R. D., Wang, Y.-K., Sherman, F., & Rustchenko, E. P. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.13.4041-4049.1999 · Cited by 141 · see citing works
Schönherr, F. A., Sparber, F., Kirchner, F. R., Guiducci, E., Trautwein-Weidner, K., Gladiator, A., Sertour, N., Hetzel, U., Le, G. T. T., Pavelka, N., et al. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.2 · Cited by 133 · see citing works
Regulation of entry into gametogenesis
van Werven, F. J., & Amon, A. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0081 · Cited by 121 · see citing works
Stress-Induced Phenotypic Switching in Candida albicans
Alby, K., & Bennett, R. J. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-01-0040 · Cited by 119 · see citing works
Self-citationBennett, R. J., Forche, A., & Berman, J. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019604 · Cited by 118 · see citing works
Self-citationChromosome instability in Candida albicans
Rustchenko, E. P. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00150.x · Cited by 117 · see citing works
Hickman, M. A., Paulson, C., Dudley, A., & Berman, J. (2015) · Genetics · doi:10.1534/genetics.115.178020 · Cited by 113 · see citing works
Heitman, J. (2015) · Fungal Biology Reviews · doi:10.1016/j.fbr.2015.08.002 · Cited by 112 · see citing works
Lockhart, S. R., Zhao, R., Daniels, K. J., & Soll, D. R. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.847-855.2003 · Cited by 107 · see citing works
Heterozygosity of genes on the sex chromosome regulates Candida albicans virulence
Wu, W., Lockhart, S. R., Pujol, C., Srikantha, T., & Soll, D. R. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05759.x · Cited by 104 · see citing works
Role of filamentation in Galleria mellonella killing by Candida albicans
Fuchs, B. B., Eby, J., Nobile, C. J., Khoury, J. B. E., Mitchell, A. P., & Mylonakis, E. E. (2010) · Microbes and Infection · doi:10.1016/j.micinf.2010.03.001 · Cited by 103 · see citing works
Infrequent Genetic Exchange and Recombination in the Mitochondrial Genome of Candida albicans
Anderson, J. B., Wickens, C., Khan, M., Cowen, L. E., Federspiel, N. A., Jones, T., & Kohn, L. M. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.3.865-872.2001 · Cited by 95 · see citing works
In Vivo and In Vitro Anaerobic Mating in Candida albicans
Dumitru, ., Navarathna, D. H. M. L. P., Semighini, C. P., Elowsky, C. G., Dumitru, R. V., Dignard, D., Whiteway, M. S., Atkin, A. L., & Nickerson, K. W. (2007) · Eukaryotic Cell · doi:10.1128/ec.00316-06 · Cited by 94 · see citing works
Fine-Resolution Physical Mapping of Genomic Diversity in Candida albicansPreprint
Chibana, H., Beckerman, J. L., & Magee, P. T. (2000) · Genome Research · doi:10.1101/gr.148600 · Cited by 88 · see citing works
Magditch, D. A., Liu, T., Xue, C., & Idnurm, A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002936 · Cited by 85 · see citing works
Aneuploidy underlies a multicellular phenotypic switch
Tan, Z., Hays, M., Cromie, G. A., Jeffery, E. W., Scott, A. C., Ahyong, V., Sirr, A., Skupin, A., & Dudley, A. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301047110 · Cited by 84 · see citing works
Chromosome 1 trisomy compromises the virulence of Candida albicans
Chen, X., Magee, B. B., Dawson, D., Magee, P. T., & Kumamoto, C. A. (2004) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03852.x · Cited by 83 · see citing works
Ploidy plasticity: a rapid and reversible strategy for adaptation to stress
Berman, J. G. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow020 · Cited by 80 · see citing works
Whole chromosome aneuploidy: Big mutations drive adaptation by phenotypic leap
Chen, G., RUBINSTEIN, B. Y., & Li, R. (2012) · BioEssays · doi:10.1002/bies.201200069 · Cited by 79 · see citing works
Does stress induce (para)sex? Implications for Candida albicans evolution
Berman, J. G., & Hadany, L. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.01.004 · Cited by 76 · see citing works
Aneuploidy and Drug Resistance in Pathogenic Fungi
Kwon-Chung, K. J., & Chang, Y. C. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003022 · Cited by 76 · see citing works
Galleria mellonellaas a model host to study virulence ofCandida
Jacobsen, I. D. (2014) · Virulence · doi:10.4161/viru.27434 · Cited by 74 · see citing works
Ploidy variation as an adaptive mechanism in human pathogenic fungi
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Panwar, S. L., Legrand, M., Dignard, D., et al. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.6.1350-1360.2003 · Cited by 70 · see citing works
Gerstein, A. C., Rosenberg, A., Hecht, I., & Berman, J. (2016) · Microbiology · doi:10.1099/mic.0.000295 · Cited by 63 · see citing works
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Wertheimer, N. B., Stone, N. R. H., & Berman, J. G. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0461 · Cited by 63 · see citing works
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Alby, K., & Bennett, R. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017234108 · Cited by 56 · see citing works
Self-citationNuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene
Bennett, R. J., Miller, M. G., Chua, P. R., et al. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04466.x · Cited by 51 · see citing works
Self-citationHao, B., Clancy, C. J., Cheng, S., Raman, S. B., Iczkowski, K. A., & Nguyen, M. H. (2009) · Eukaryotic Cell · doi:10.1128/ec.00246-08 · Cited by 46 · see citing works
Gerstein, A. C., Lim, H., Berman, J. G., & Hickman, M. A. (2017) · Evolution · doi:10.1111/evo.13205 · Cited by 43 · see citing works
Alby, K., & Bennett, R. J. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0421-8 · Cited by 40 · see citing works
Self-citationSun, S., & Heitman, J. (2011) · BMC Biology · doi:10.1186/1741-7007-9-56 · Cited by 38 · see citing works
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Zhang, N., Magee, B. B., Magee, P. T., Holland, B. R., Rodrigues, E., Holmes, A. R., Cannon, R. D., & Schmid, J. (2015) · Genetics · doi:10.1534/genetics.115.177170 · Cited by 28 · see citing works
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Zeng, G., Wang, Y., Chan, F. Y., & Wang, Y. (2014) · Nature Protocols · doi:10.1038/nprot.2014.029 · Cited by 24 · see citing works
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Antifungal Drug Resistance: Molecular Mechanisms in <i>Candida albicans</i> and Beyond
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Forche, A., Cromie, G., Gerstein, A. C., Solis, N. V., Pisithkul, T., Srifa, W., Jeffery, E., Abbey, D., Filler, S. G., Dudley, A. M., et al. (2018) · Genetics · doi:10.1534/genetics.118.301019 · Cited by 94 · see citing works
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Vande Zande, P., Zhou, X., & Selmecki, A. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-041320-112443 · Cited by 70 · see citing works
Within-Host Genomic Diversity of Candida albicans in Healthy Carriers
Sitterlé, E., Maufrais, C., Sertour, N., Palayret, M., d’Enfert, C., & Bougnoux, M.-E. (2019) · Scientific Reports · doi:10.1038/s41598-019-38768-4 · Cited by 51 · see citing works
Mba, I. E., Nweze, E. I., Eze, E. A., & Anyaegbunam, Z. K. G. (2022) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2022.105256 · Cited by 46 · see citing works
- Authors
- Hirakawa, M. P., Chyou, D. E., Huang, D., Slan, A. R., & Bennett, R. J.
- Affiliations
- Brown University (US)
- Corresponding author
- Bennett, Richard J
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-09-14
- Volume
- 207
- Issue
- 3
- Pages
- 1195-1211
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC5676243
- OpenAlex
- W2756439128
- Cited by
- 47
- References
- 110
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 7 · 2021: 5 · 2020: 7 · 2019: 10 · 2018: 6
- FWCI
- 2.57
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Burroughs Wellcome Fund
- Broad Institute
- University of Aberdeen
- National Institutes of Health (5r01ai081704-12, AI081704)
- National Institute of Allergy and Infectious Diseases (R01-AI081704, R21AI112363)
- National Institute of Dental and Craniofacial Research (F31DE023726)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Keywords
- Candida albicans, parasexual cycle, phenotypic diversity, drug resistance, fluconazole resistance, virulence, aneuploidy, chromosome loss, homothallism, filamentation, biofilm formation, Galleria mellonella infection model, fitness, diploidy
- MeSH terms
- Antifungal Agents, Candida, Cell Division, Phenotype, Ploidies, Genetic Variation, Virulence, Fluconazole, Drug Resistance, Fungal
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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