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Chapter 28 : Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution

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Abstract:

Cellular ploidy is the number of complete sets of chromosomes in a cell. Many eukaryotic species have two (diploid) or more than two (polyploid) sets of chromosomes ( ). These diploid and polyploid states are often the result of ancient whole-genome duplication (WGD) or hybridization events that occurred throughout the evolution of plants, animals, and fungi ( ). Ploidy changes also occur during the development of many organisms and can vary within different tissues of the same organism and between individuals of the same species. For example, ploidy changes occur during the sexual cycle of eukaryotes, from haploid gametes to diploid somatic cells. Additionally, some cells continue to increase in ploidy during development, resulting in somatic tissues that have a mixture of diploid and polyploid cells, including human hepatocytes and megakaryocytes ( ). These ongoing, developmentally programmed changes in ploidy are important for viability and are beneficial to many organisms ( ), but the mechanisms controlling ploidy and the physiological significance of each ploidy level are not well characterized.

Citation: Todd R, Forche A, Selmecki A. 2017. Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution, p 599-618. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0051-2016
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Figure 1

Methods for detection of ploidy and aneuploidy. Ploidy is determined with flow cytometry. Total genome fluorescence, measured using a fluorescent nucleotide label (e.g., propidium iodide or Sytox Green). Cells are first fixed (in ethanol) and RNA is removed with RNase, then genomic DNA is fluorescently labeled and analyzed on a flow cytometer. Cells are passed through a laser, and the number of cells are plotted as a function of fluorescence intensity. Cells in a population typically have two fluorescent peaks, representing cells in either G1 or G2 phases of the cell cycle. Flow cytometry plots for yeast with the following ploidy levels are shown: haploid (1N), diploid (2N), triploid (3N), tetraploid (4N), and a near-tetraploid aneuploid. Chromosome copy number is determined with WGS and microarray aCGH. The axis represents a log fold change of sequence reads relative to the reference sequence and chromosome number increases from left to right starting with chromosome I and ending with chromosome XVI ( axis). Chromosome copy number plots for with the following ploidy levels indicate euploid genome for haploid (1N), diploid (2N), triploid (3N), and tetraploid (4N). However, the near-tetraploid isolate (bottom panel) is aneuploid for ChrXII (pentasomic) and ChrXIV (trisomic) and contains a segmental aneuploidy of ChrIV. Figures generated from data obtained in reference . Allele frequencies obtained from WGS data also can be used to determine the ploidy of a strain. The axis shows the heterozygous allele frequencies ranging from zero to one, plotted as a function of chromosome number starting with chromosome I and ending with chromosome XVI ( axis). Allele frequency plot of the example haploid strain with single nucleotide polymorphisms (SNPs) at allele frequencies at 1.0; a diploid strain with SNPs at allele frequencies of 0.5 and 1.0; a triploid strain with SNPs at allele frequencies of 0.33 and 0.66; and a tetraploid strain with SNPs at allele frequencies at 0.25, 0.5, 0.75, and 1.0. Images obtained from reference . A diploid strain that is trisomic (three copies of a chromosome) for chromosome XII (left panel). Interestingly, the allele frequency plot has SNPs at allele frequencies of 0.5 and 1.0 for all chromosomes except ChrXII, which is at allele frequencies of 0.33 and 0.66, supporting that this chromosome is aneuploid (right panel).

Citation: Todd R, Forche A, Selmecki A. 2017. Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution, p 599-618. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0051-2016
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Figure 2

Many polyploid-evolved clones are highly aneuploid. Chromosome copy number was determined by WGS and plotted for the parental diploid (2N) and tetraploid (4N) strains and different tetraploid evolved clones after 250 generations in raffinose medium. Adaptation resulted in clones with increased chromosome copies, approximately trisomic copies of every chromosome (∼3N), or highly aneuploid genomes. Figures generated from data obtained from the supplementary data Table 1 in reference .

Citation: Todd R, Forche A, Selmecki A. 2017. Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution, p 599-618. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0051-2016
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References

/content/book/10.1128/9781555819583.chap28
1. Otto SP,, Whitton J . 2000. Polyploid incidence and evolution. Annu Rev Genet 34 : 401437.[CrossRef] [PubMed]
2. Otto SP . 2007. The evolutionary consequences of polyploidy. Cell 131 : 452462.[CrossRef]
3. Sémon M,, Wolfe KH . 2007. Consequences of genome duplication. Curr Opin Genet Dev 17 : 505512.[CrossRef] [PubMed]
4. Albertin W,, Marullo P . 2012. Polyploidy in fungi: evolution after whole-genome duplication. Proc Biol Sci 279 : 24972509.[CrossRef] [PubMed]
5. Garcia AM . 1964. Studies on DNA in leucocytes and related cells of mammals. IV. The feulgen-DNA content of peripheral leucocytes, megakaryocytes and other bone marrow cell types of the rabbit. Acta Histochem 17 : 246258.[PubMed]
6. Wheatley DN . 1972. Binucleation in mammalian liver: studies on the control of cytokinesis in vivo . Exp Cell Res 74 : 455465.[CrossRef] [PubMed]
7. Nadal C,, Zajdela F . 1967. Hepatic polyploidy in the rat. IV. Experimental changes in the nucleolar volume of liver cells and their mechanisms of regulation. Exp Cell Res 48 : 518528. (In Greek, Modern.)[CrossRef]
8. Duncan AW,, Taylor MH,, Hickey RD,, Hanlon Newell AE,, Lenzi ML,, Olson SB,, Finegold MJ,, Grompe M . 2010. The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 467 : 707710.[CrossRef]
9. Bennett RJ,, Johnson AD . 2003. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J 22 : 25052515.[CrossRef]
10. Suzuki T,, Nishibayashi S,, Kuroiwa T,, Kanbe T,, Tanaka K . 1982. Variance of ploidy in Candida albicans . J Bacteriol 152 : 893896.[PubMed]
11. Suzuki T,, Hitomi A,, Magee PT,, Sakaguchi S . 1994. Correlation between polyploidy and auxotrophic segregation in the imperfect yeast Candida albicans . J Bacteriol 176 : 33453353.[CrossRef]
12. Ezov TK,, Boger-Nadjar E,, Frenkel Z,, Katsperovski I,, Kemeny S,, Nevo E,, Korol A,, Kashi Y . 2006. Molecular-genetic biodiversity in a natural population of the yeast Saccharomyces cerevisiae from “Evolution Canyon”: microsatellite polymorphism, ploidy and controversial sexual status. Genetics 174 : 14551468.[CrossRef]
13. Selmecki A,, Gerami-Nejad M,, Paulson C,, Forche A,, Berman J . 2008. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 68 : 624641.[CrossRef]
14. Dunn B,, Richter C,, Kvitek DJ,, Pugh T,, Sherlock G . 2012. Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res 22 : 908924.[CrossRef]
15. Ford CB,, Funt JM,, Abbey D,, Issi L,, Guiducci C,, Martinez DA,, Delorey T,, Li BY,, White TC,, Cuomo C,, Rao RP,, Berman J,, Thompson DA,, Regev A . 2015. The evolution of drug resistance in clinical isolates of Candida albicans . eLife 4 : e00662.[CrossRef] [PubMed]
16. Zhu YO,, Sherlock G,, Petrov DA . 2016. Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation. G3 (Bethesda) 6 : 24212434.[CrossRef]
17. Zörgö E,, Chwialkowska K,, Gjuvsland AB,, Garré E,, Sunnerhagen P,, Liti G,, Blomberg A,, Omholt SW,, Warringer J . 2013. Ancient evolutionary trade-offs between yeast ploidy states. PLoS Genet 9 : e1003388.[CrossRef]
18. Dufresne F,, Stift M,, Vergilino R,, Mable BK . 2014. Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Mol Ecol 23 : 4069.[CrossRef]
19. Gerstein AC,, Chun HJ,, Grant A,, Otto SP . 2006. Genomic convergence toward diploidy in Saccharomyces cerevisiae . PLoS Genet 2 : e145.[CrossRef]
20. Selmecki AM,, Maruvka YE,, Richmond PA,, Guillet M,, Shoresh N,, Sorenson AL,, De S,, Kishony R,, Michor F,, Dowell R,, Pellman D . 2015. Polyploidy can drive rapid adaptation in yeast. Nature 519 : 349352.[CrossRef] [PubMed]
21. Venkataram S,, Dunn B,, Li Y,, Agarwala A,, Chang J,, Ebel ER,, Geiler-Samerotte K,, Herissant L,, Blundell JR,, Levy SF,, Fisher DS,, Sherlock G,, Petrov DA . 2016. Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166 : 15851596.[PubMed]
22. Krishan A . 1975. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J Cell Biol 66 : 188193.[CrossRef] [PubMed]
23. Pinkel D,, Segraves R,, Sudar D,, Clark S,, Poole I,, Kowbel D,, Collins C,, Kuo WL,, Chen C,, Zhai Y,, Dairkee SH,, Ljung BM,, Gray JW,, Albertson DG . 1998. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 20 : 207211.[CrossRef]
24. Wilhelm J,, Pingoud A,, Hahn M . 2003. Validation of an algorithm for automatic quantification of nucleic acid copy numbers by real-time polymerase chain reaction. Anal Biochem 317 : 218225.[CrossRef]
25. Peterson BK,, Weber JN,, Kay EH,, Fisher HS,, Hoekstra HE . 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7 : e37135.[CrossRef]
26. Gompert Z,, Mock KE . 2017. Detection of individual ploidy levels with genotyping-by-sequencing (GBS) analysis. Mol Ecol Resour.[CrossRef] [PubMed]
27. Liti G . 2015. The fascinating and secret wild life of the budding yeast S. cerevisiae . eLife 4 : 4.[CrossRef]
28. Carreto L,, Eiriz MF,, Gomes AC,, Pereira PM,, Schuller D,, Santos MA . 2008. Comparative genomics of wild type yeast strains unveils important genome diversity. BMC Genomics 9 : 524.[CrossRef]
29. Strope PK,, Skelly DA,, Kozmin SG,, Mahadevan G,, Stone EA,, Magwene PM,, Dietrich FS,, McCusker JH . 2015. The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res 25 : 762774.[CrossRef]
30. Albertin W,, Marullo P,, Aigle M,, Bourgais A,, Bely M,, Dillmann C,, DE Vienne D,, Sicard D . 2009. Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: towards a new domesticated species. J Evol Biol 22 : 21572170.[CrossRef]
31. Lindell RM,, Hartman TE,, Nadrous HF,, Ryu JH . 2005. Pulmonary cryptococcosis: CT findings in immunocompetent patients. Radiology 236 : 326331.[CrossRef]
32. Tien RD,, Chu PK,, Hesselink JR,, Duberg A,, Wiley C . 1991. Intracranial cryptococcosis in immunocompromised patients: CT and MR findings in 29 cases. AJNR Am J Neuroradiol 12 : 283289.[PubMed]
33. Velagapudi R,, Hsueh YP,, Geunes-Boyer S,, Wright JR,, Heitman J . 2009. Spores as infectious propagules of Cryptococcus neoformans . Infect Immun 77 : 43454355.[CrossRef]
34. Idnurm A,, Verma S,, Corrochano LM . 2010. A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol 47 : 881892.[CrossRef]
35. Ni M,, Feretzaki M,, Li W,, Floyd-Averette A,, Mieczkowski P,, Dietrich FS,, Heitman J . 2013. Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans . PLoS Biol 11 : e1001653.[CrossRef]
36. Feldmesser M,, Kress Y,, Casadevall A . 2001. Dynamic changes in the morphology of Cryptococcus neoformans during murine pulmonary infection. Microbiology 147 : 23552365.[CrossRef]
37. Ene IV,, Bennett RJ . 2014. The cryptic sexual strategies of human fungal pathogens. Nat Rev Microbiol 12 : 239251.[CrossRef]
38. Okagaki LH,, Strain AK,, Nielsen JN,, Charlier C,, Baltes NJ,, Chrétien F,, Heitman J,, Dromer F,, Nielsen K . 2010. Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6 : e1000953.[CrossRef] [PubMed]
39. Zaragoza O,, García-Rodas R,, Nosanchuk JD,, Cuenca-Estrella M,, Rodríguez-Tudela JL,, Casadevall A . 2010. Fungal cell gigantism during mammalian infection. PLoS Pathog 6 : e1000945.[CrossRef]
40. Sallé J,, Campbell SD,, Gho M,, Audibert A . 2012. CycA is involved in the control of endoreplication dynamics in the Drosophila bristle lineage. Development 139 : 547557.[CrossRef] [PubMed]
41. Dudas J,, Saile B,, El-Armouche H,, Aprigliano I,, Ramadori G . 2003. Endoreplication and polyploidy in primary culture of rat hepatic stellate cells. Cell Tissue Res 313 : 301311.[CrossRef]
42. Sionov E,, Lee H,, Chang YC,, Kwon-Chung KJ . 2010. Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog 6 : e1000848.[CrossRef]
43. Gerstein AC,, Fu MS,, Mukaremera L,, Li Z,, Ormerod KL,, Fraser JA,, Berman J,, Nielsen K . 2015. Polyploid titan cells produce haploid and aneuploid progeny to promote stress adaptation. MBio 6 : e01340-15.[CrossRef]
44. Riggsby WS,, Torres-Bauza LJ,, Wills JW,, Townes TM . 1982. DNA content, kinetic complexity, and the ploidy question in Candida albicans . Mol Cell Biol 2 : 853862.[CrossRef] [PubMed]
45. Jones T,, Federspiel NA,, Chibana H,, Dungan J,, Kalman S,, Magee BB,, Newport G,, Thorstenson YR,, Agabian N,, Magee PT,, Davis RW,, Scherer S . 2004. The diploid genome sequence of Candida albicans . Proc Natl Acad Sci USA 101 : 73297334.[CrossRef] [PubMed]
46. Selmecki A,, Forche A,, Berman J . 2010. Genomic plasticity of the human fungal pathogen Candida albicans . Eukaryot Cell 9 : 9911008.[CrossRef]
47. Hickman MA,, Zeng G,, Forche A,, Hirakawa MP,, Abbey D,, Harrison BD,, Wang YM,, Su CH,, Bennett RJ,, Wang Y,, Berman J . 2013. The ‘obligate diploid’ Candida albicans forms mating-competent haploids. Nature 494 : 5559.[CrossRef]
48. Abbey DA,, Funt J,, Lurie-Weinberger MN,, Thompson DA,, Regev A,, Myers CL,, Berman J . 2014. YMAP: a pipeline for visualization of copy number variation and loss of heterozygosity in eukaryotic pathogens. Genome Med 6 : 100.
49. 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 . 2001. Genomic evidence for a complete sexual cycle in Candida albicans . Proc Natl Acad Sci USA 98 : 32493253.[CrossRef]
50. Hull CM,, Johnson AD . 1999. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans . Science 285 : 12711275.[CrossRef]
51. Magee BB,, Magee PT . 2000. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289 : 310313.[CrossRef] [PubMed]
52. Forche A,, Alby K,, Schaefer D,, Johnson AD,, Berman J,, Bennett RJ . 2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6 : e110.[CrossRef]
53. Alby K,, Schaefer D,, Bennett RJ . 2009. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans . Nature 460 : 890893.[CrossRef] [PubMed]
54. Hickman MA,, Paulson C,, Dudley A,, Berman J . 2015. Parasexual ploidy reduction drives population heterogeneity through random and transient aneuploidy in Candida albicans . Genetics 200 : 781794.[CrossRef]
55. Hilton C,, Markie D,, Corner B,, Rikkerink E,, Poulter R . 1985. Heat shock induces chromosome loss in the yeast Candida albicans . Mol Gen Genet 200 : 162168.[CrossRef]
56. Janbon G,, Sherman F,, Rustchenko E . 1998. Monosomy of a specific chromosome determines L-sorbose utilization: a novel regulatory mechanism in Candida albicans . Proc Natl Acad Sci USA 95 : 51505155.[CrossRef]
57. Kabir MA,, Ahmad A,, Greenberg JR,, Wang YK,, Rustchenko E . 2005. Loss and gain of chromosome 5 controls growth of Candida albicans on sorbose due to dispersed redundant negative regulators. Proc Natl Acad Sci USA 102 : 1214712152. (Erratum, doi:10.1073/pnas.0507247102.)[CrossRef]
58. Forche A,, May G,, Magee PT . 2005. Demonstration of loss of heterozygosity by single-nucleotide polymorphism microarray analysis and alterations in strain morphology in Candida albicans strains during infection. Eukaryot Cell 4 : 156165.[CrossRef]
59. Selmecki A,, Forche A,, Berman J . 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans . Science 313 : 367370.[CrossRef]
60. Forche A,, Magee PT,, Selmecki A,, Berman J,, May G . 2009. Evolution in Candida albicans populations during a single passage through a mouse host. Genetics 182 : 799811.[CrossRef]
61. Selmecki AM,, Dulmage K,, Cowen LE,, Anderson JB,, Berman J . 2009. Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet 5 : e1000705.[CrossRef]
62. Harrison BD,, Hashemi J,, Bibi M,, Pulver R,, Bavli D,, Nahmias Y,, Wellington M,, Sapiro G,, Berman J . 2014. A tetraploid intermediate precedes aneuploid formation in yeasts exposed to fluconazole. PLoS Biol 12 : e1001815.[CrossRef]
63. Anderson CA,, Roberts S,, Zhang H,, Kelly CM,, Kendall A,, Lee C,, Gerstenberger J,, Koenig AB,, Kabeche R,, Gladfelter AS . 2015. Ploidy variation in multinucleate cells changes under stress. Mol Biol Cell 26 : 11291140.[CrossRef]
64. Farrer RA,, Henk DA,, Garner TW,, Balloux F,, Woodhams DC,, Fisher MC . 2013. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet 9 : e1003703.[CrossRef]
65. Vlaardingerbroek I,, Beerens B,, Schmidt SM,, Cornelissen BJ,, Rep M . 2016. Dispensable chromosomes in Fusarium oxysporum f. sp. lycopersici . Mol Plant Pathol 17 : 14551466.[CrossRef] [PubMed]
66. Kasuga T,, Bui M,, Bernhardt E,, Swiecki T,, Aram K,, Cano LM,, Webber J,, Brasier C,, Press C,, Grünwald NJ,, Rizzo DM,, Garbelotto M . 2016. Host-induced aneuploidy and phenotypic diversification in the sudden oak death pathogen Phytophthora ramorum . BMC Genomics 17 : 385.[CrossRef]
67. Chan CS,, Botstein D . 1993. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 135 : 677691.[PubMed]
68. Porter AC . 2008. Preventing DNA over-replication: a Cdk perspective. Cell Div 3 : 3.[CrossRef]
69. Edgar BA,, Orr-Weaver TL . 2001. Endoreplication cell cycles: more for less. Cell 105 : 297306.[CrossRef]
70. Neiman M,, Beaton MJ,, Hessen DO,, Jeyasingh PD,, Weider LJ . 2017. Endopolyploidy as a potential driver of animal ecology and evolution. Biol Rev Camb Philos Soc 92 : 234247.[CrossRef]
71. Hayles J,, Fisher D,, Woollard A,, Nurse P . 1994. Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 78 : 813822.[CrossRef] [PubMed]
72. Vassilev A,, Lee CY,, Vassilev B,, Zhu W,, Ormanoglu P,, Martin SE,, DePamphilis ML . 2016. Identification of genes that are essential to restrict genome duplication to once per cell division. Oncotarget 7 : 3495634976.[PubMed]
73. Duncan AW . 2013. Aneuploidy, polyploidy and ploidy reversal in the liver. Semin Cell Dev Biol 24 : 347356.[CrossRef] [PubMed]
74. Guidotti JE,, Brégerie O,, Robert A,, Debey P,, Brechot C,, Desdouets C . 2003. Liver cell polyploidization: a pivotal role for binuclear hepatocytes. J Biol Chem 278 : 1909519101.[CrossRef]
75. Margall-Ducos G,, Celton-Morizur S,, Couton D,, Brégerie O,, Desdouets C . 2007. Liver tetraploidization is controlled by a new process of incomplete cytokinesis. J Cell Sci 120 : 36333639.[CrossRef]
76. Winey M,, Hoyt MA,, Chan C,, Goetsch L,, Botstein D,, Byers B . 1993. NDC1: a nuclear periphery component required for yeast spindle pole body duplication. J Cell Biol 122 : 743751.[CrossRef]
77. Biggins S,, Severin FF,, Bhalla N,, Sassoon I,, Hyman AA,, Murray AW . 1999. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13 : 532544.[CrossRef]
78. Francisco L,, Chan CS . 1994. Regulation of yeast chromosome segregation by Ipl1 protein kinase and type 1 protein phosphatase. Cell Mol Biol Res 40 : 207213.[PubMed]
79. He X,, Rines DR,, Espelin CW,, Sorger PK . 2001. Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell 106 : 195206.[CrossRef]
80. Guacci V,, Koshland D,, Strunnikov A . 1997. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae . Cell 91 : 4757.[CrossRef]
81. Covo S,, Puccia CM,, Argueso JL,, Gordenin DA,, Resnick MA . 2014. The sister chromatid cohesion pathway suppresses multiple chromosome gain and chromosome amplification. Genetics 196 : 373384.[CrossRef]
82. Yu Y,, Srinivasan M,, Nakanishi S,, Leatherwood J,, Shilatifard A,, Sternglanz R . 2011. A conserved patch near the C terminus of histone H4 is required for genome stability in budding yeast. Mol Cell Biol 31 : 23112325.[CrossRef]
83. Albert I,, Mavrich TN,, Tomsho LP,, Qi J,, Zanton SJ,, Schuster SC,, Pugh BF . 2007. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446 : 572576.[CrossRef]
84. Chambers AL,, Ormerod G,, Durley SC,, Sing TL,, Brown GW,, Kent NA,, Downs JA . 2012. The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev 26 : 25902603.[CrossRef]
85. Watts FZ,, Shiels G,, Orr E . 1987. The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J 6 : 34993505.[PubMed]
86. Rancati G,, Pavelka N,, Fleharty B,, Noll A,, Trimble R,, Walton K,, Perera A,, Staehling-Hampton K,, Seidel CW,, Li R . 2008. Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135 : 879893.[CrossRef]
87. Song W,, Petes TD . 2012. Haploidization in Saccharomyces cerevisiae induced by a deficiency in homologous recombination. Genetics 191 : 279284.[CrossRef]
88. Storchová Z,, Breneman A,, Cande J,, Dunn J,, Burbank K,, O’Toole E,, Pellman D . 2006. Genome-wide genetic analysis of polyploidy in yeast. Nature 443 : 541547.[CrossRef] [PubMed]
89. Alabrudzinska M,, Skoneczny M,, Skoneczna A . 2011. Diploid-specific [corrected] genome stability genes of S. cerevisiae: genomic screen reveals haploidization as an escape from persisting DNA rearrangement stress. PLoS One 6 : e21124.[CrossRef]
90. Haber JE . 1992. Exploring the pathways of homologous recombination. Curr Opin Cell Biol 4 : 401412.[CrossRef]
91. Mehta A,, Beach A,, Haber JE . 2017. Homology requirements and competition between gene conversion and break-induced replication during double-strand break repair. Mol Cell 65 : 515526.[PubMed]
92. Chen C,, Kolodner RD . 1999. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat Genet 23 : 8185.[CrossRef]
93. Hiraoka M,, Watanabe K,, Umezu K,, Maki H . 2000. Spontaneous loss of heterozygosity in diploid Saccharomyces cerevisiae cells. Genetics 156 : 15311548.[PubMed]
94. Skoneczna A,, Kaniak A,, Skoneczny M . 2015. Genetic instability in budding and fission yeast-sources and mechanisms. FEMS Microbiol Rev 39 : 917967.[CrossRef] [PubMed]
95. Ohnishi G,, Endo K,, Doi A,, Fujita A,, Daigaku Y,, Nunoshiba T,, Yamamoto K . 2004. Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae . Biochem Biophys Res Commun 325 : 928933.[CrossRef]
96. Jung PP,, Fritsch ES,, Blugeon C,, Souciet JL,, Potier S,, Lemoine S,, Schacherer J,, de Montigny J . 2011. Ploidy influences cellular responses to gross chromosomal rearrangements in Saccharomyces cerevisiae . BMC Genomics 12 : 331.[CrossRef]
97. Storchova Z,, Kuffer C . 2008. The consequences of tetraploidy and aneuploidy. J Cell Sci 121 : 38593866.[CrossRef]
98. Matzke MA,, Mittelsten Scheid O,, Matzke AJ . 1999. Rapid structural and epigenetic changes in polyploid and aneuploid genomes. BioEssays 21 : 761767.[CrossRef]
99. Comai L . 2005. The advantages and disadvantages of being polyploid. Nat Rev Genet 6 : 836846.[CrossRef]
100. Comai L,, Tyagi AP,, Winter K,, Holmes-Davis R,, Reynolds SH,, Stevens Y,, Byers B . 2000. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12 : 15511568.[CrossRef]
101. Hufton AL,, Panopoulou G . 2009. Polyploidy and genome restructuring: a variety of outcomes. Curr Opin Genet Dev 19 : 600606.[CrossRef]
102. Mayer VW,, Aguilera A . 1990. High levels of chromosome instability in polyploids of Saccharomyces cerevisiae . Mutat Res 231 : 177186.[CrossRef] [PubMed]
103. Andalis AA,, Storchova Z,, Styles C,, Galitski T,, Pellman D,, Fink GR . 2004. Defects arising from whole-genome duplications in Saccharomyces cerevisiae . Genetics 167 : 11091121.[CrossRef]
104. Seervai RN,, Jones SK Jr,, Hirakawa MP,, Porman AM,, Bennett RJ . 2013. Parasexuality and ploidy change in Candida tropicalis . Eukaryot Cell 12 : 16291640.[CrossRef] [PubMed]
105. Gerstein AC,, McBride RM,, Otto SP . 2008. Ploidy reduction in Saccharomyces cerevisiae . Biol Lett 4 : 9194.[CrossRef]
106. Levine DS,, Sanchez CA,, Rabinovitch PS,, Reid BJ . 1991. Formation of the tetraploid intermediate is associated with the development of cells with more than four centrioles in the elastase-simian virus 40 tumor antigen transgenic mouse model of pancreatic cancer. Proc Natl Acad Sci USA 88 : 64276431.[CrossRef]
107. Lu YJ,, Swamy KB,, Leu JY . 2016. Experimental evolution reveals interplay between Sch9 and polyploid stability in yeast. PLoS Genet 12 : e1006409.[CrossRef]
108. Miettinen TP,, Pessa HK,, Caldez MJ,, Fuhrer T,, Diril MK,, Sauer U,, Kaldis P,, Björklund M . 2014. Identification of transcriptional and metabolic programs related to mammalian cell size. Curr Biol 24 : 598608.[CrossRef] [PubMed]
109. Wu CY,, Rolfe PA,, Gifford DK,, Fink GR . 2010. Control of transcription by cell size. PLoS Biol 8 : e1000523.[CrossRef]
110. Watanabe T,, Tanaka Y . 1982. Age-related alterations in the size of human hepatocytes. A study of mononuclear and binucleate cells. Virchows Arch B Cell Pathol Incl Mol Pathol 39 : 920.[CrossRef]
111. Conlon I,, Raff M . 1999. Size control in animal development. Cell 96 : 235244.[CrossRef]
112. Tsukaya H . 2013. Does ploidy level directly control cell size? Counterevidence from Arabidopsis genetics. PLoS One 8 : e83729.[CrossRef] [PubMed]
113. Weiss RL,, Kukora JR,, Adams J . 1975. The relationship between enzyme activity, cell geometry, and fitness in Saccharomyces cerevisiae . Proc Natl Acad Sci USA 72 : 794798.[CrossRef]
114. Galitski T,, Saldanha AJ,, Styles CA,, Lander ES,, Fink GR . 1999. Ploidy regulation of gene expression. Science 285 : 251254.[CrossRef]
115. Mable BK,, Otto SP . 2001. Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet Res 77 : 926.[CrossRef]
116. Dowell RD,, Ryan O,, Jansen A,, Cheung D,, Agarwala S,, Danford T,, Bernstein DA,, Rolfe PA,, Heisler LE,, Chin B,, Nislow C,, Giaever G,, Phillips PC,, Fink GR,, Gifford DK,, Boone C . 2010. Genotype to phenotype: a complex problem. Science 328 : 469.[CrossRef]
117. de Godoy LM,, Olsen JV,, Cox J,, Nielsen ML,, Hubner NC,, Fröhlich F,, Walther TC,, Mann M . 2008. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455 : 12511254.[CrossRef]
118. Voordeckers K,, Kominek J,, Das A,, Espinosa-Cantú A,, De Maeyer D,, Arslan A,, Van Pee M,, van der Zande E,, Meert W,, Yang Y,, Zhu B,, Marchal K,, DeLuna A,, Van Noort V,, Jelier R,, Verstrepen KJ . 2015. Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet 11 : e1005635.[CrossRef]
119. Levy SF,, Blundell JR,, Venkataram S,, Petrov DA,, Fisher DS,, Sherlock G . 2015. Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519 : 181186.[CrossRef]
120. Bouchonville K,, Forche A,, Tang KE,, Selmecki A,, Berman J . 2009. Aneuploid chromosomes are highly unstable during DNA transformation of Candida albicans . Eukaryot Cell 8 : 15541566.[PubMed]
121. Gerstein AC,, Lim H,, Berman J,, Hickman MA . 2017. Ploidy tug-of-war: evolutionary and genetic environments influence the rate of ploidy drive in a human fungal pathogen. Evolution 71 : 10251038.[CrossRef]
122. Coste A,, Selmecki A,, Forche A,, Diogo D,, Bougnoux ME,, d’Enfert C,, Berman J,, Sanglard D . 2007. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6 : 18891904.[CrossRef]
123. Chang FM,, Ou TY,, Cheng WN,, Chou ML,, Lee KC,, Chin YP,, Lin CP,, Chang KD,, Lin CT,, Su CH . 2014. Short-term exposure to fluconazole induces chromosome loss in Candida albicans: an approach to produce haploid cells. Fungal Genet Biol 70 : 6876.[CrossRef]
124. Ngamskulrungroj P,, Chang Y,, Hansen B,, Bugge C,, Fischer E,, Kwon-Chung KJ . 2012. Characterization of the chromosome 4 genes that affect fluconazole-induced disomy formation in Cryptococcus neoformans . PLoS One 7 : e33022.[CrossRef]
125. Yona AH,, Manor YS,, Herbst RH,, Romano GH,, Mitchell A,, Kupiec M,, Pilpel Y,, Dahan O . 2012. Chromosomal duplication is a transient evolutionary solution to stress. Proc Natl Acad Sci USA 109 : 2101021015.[CrossRef]
126. Torres EM,, Sokolsky T,, Tucker CM,, Chan LY,, Boselli M,, Dunham MJ,, Amon A . 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317 : 916924.[CrossRef] [PubMed]
127. Lingelbach LB,, Kaplan KB . 2004. The interaction between Sgt1p and Skp1p is regulated by HSP90 chaperones and is required for proper CBF3 assembly. Mol Cell Biol 24 : 89388950.[CrossRef]
128. Chen G,, Bradford WD,, Seidel CW,, Li R . 2012. Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature 482 : 246250.
129. Sunshine AB,, Payen C,, Ong GT,, Liachko I,, Tan KM,, Dunham MJ . 2015. The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biol 13 : e1002155.[CrossRef]
130. Payen C,, Sunshine AB,, Ong GT,, Pogachar JL,, Zhao W,, Dunham MJ . 2016. High-throughput identification of adaptive mutations in experimentally evolved yeast populations. PLoS Genet 12 : e1006339.[CrossRef]
131. Gresham D,, Desai MM,, Tucker CM,, Jenq HT,, Pai DA,, Ward A,, DeSevo CG,, Botstein D,, Dunham MJ . 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4 : e1000303.[CrossRef]
132. Croll D,, McDonald BA . 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog 8 : e1002608.[CrossRef]
133. Wittenberg AH,, van der Lee TA,, Ben M’barek S,, Ware SB,, Goodwin SB,, Kilian A,, Visser RG,, Kema GH,, Schouten HJ . 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola . PLoS One 4 : e5863.[CrossRef]
134. Van de Wouw AP,, Cozijnsen AJ,, Hane JK,, Brunner PC,, McDonald BA,, Oliver RP,, Howlett BJ . 2010. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6 : e1001180.[CrossRef]
135. Raffaele S,, Farrer RA,, Cano LM,, Studholme DJ,, MacLean D,, Thines M,, Jiang RH,, Zody MC,, Kunjeti SG,, Donofrio NM,, Meyers BC,, Nusbaum C,, Kamoun S . 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330 : 15401543.[CrossRef]
136. Coleman JJ,, Rounsley SD,, Rodriguez-Carres M,, Kuo A,, Wasmann CC,, Grimwood J,, Schmutz J,, Taga M,, White GJ,, Zhou S,, Schwartz DC,, Freitag M,, Ma LJ,, Danchin EG,, Henrissat B,, Coutinho PM,, Nelson DR,, Straney D,, Napoli CA,, Barker BM,, Gribskov M,, Rep M,, Kroken S,, Molnár I,, Rensing C,, Kennell JC,, Zamora J,, Farman ML,, Selker EU,, Salamov A,, Shapiro H,, Pangilinan J,, Lindquist E,, Lamers C,, Grigoriev IV,, Geiser DM,, Covert SF,, Temporini E,, Vanetten HD . 2009. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5 : e1000618.[CrossRef]
137. Miao VP,, Covert SF,, VanEtten HD . 1991. A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254 : 17731776.[CrossRef]
138. Ma LJ , , et al . 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium . Nature 464 : 367373.[CrossRef]
139. Roper M,, Ellison C,, Taylor JW,, Glass NL . 2011. Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr Biol 21 : R786R793.[CrossRef]
140. Rustchenko-Bulgac EP . 1991. Variations of Candida albicans electrophoretic karyotypes. J Bacteriol 173 : 65866596.[CrossRef] [PubMed]
141. Ahmad KM,, Kokošar J,, Guo X,, Gu Z,, Ishchuk OP,, Piškur J . 2014. Genome structure and dynamics of the yeast pathogen Candida glabrata . FEMS Yeast Res 14 : 529535.[CrossRef] [PubMed]
142. Sem X,, Le GT,, Tan AS,, Tso G,, Yurieva M,, Liao WW,, Lum J,, Srinivasan KG,, Poidinger M,, Zolezzi F,, Pavelka N . 2016. Beta-glucan exposure on the fungal cell wall tightly correlates with competitive fitness of Candida species in the mouse gastrointestinal tract. Front Cell Infect Microbiol 6 : 186.[CrossRef]
143. Zaragoza O,, Nielsen K . 2013. Titan cells in Cryptococcus neoformans: cells with a giant impact. Curr Opin Microbiol 16 : 409413.[CrossRef]
144. Lin X,, Patel S,, Litvintseva AP,, Floyd A,, Mitchell TG,, Heitman J . 2009. Diploids in the Cryptococcus neoformans serotype A population homozygous for the alpha mating type originate via unisexual mating. PLoS Pathog 5 : e1000283.[CrossRef]
145. Zaragoza O,, Fries BC,, Casadevall A . 2003. Induction of capsule growth in Cryptococcus neoformans by mammalian serum and CO(2). Infect Immun 71 : 61556164.[CrossRef]
146. Kronstad JW,, Attarian R,, Cadieux B,, Choi J,, D’Souza CA,, Griffiths EJ,, Geddes JM,, Hu G,, Jung WH,, Kretschmer M,, Saikia S,, Wang J . 2011. Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat Rev Microbiol 9 : 193203.[CrossRef]
147. Paquin C,, Adams J . 1983. Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302 : 495500.[CrossRef]
148. DeLuna A,, Vetsigian K,, Shoresh N,, Hegreness M,, Colón-González M,, Chao S,, Kishony R . 2008. Exposing the fitness contribution of duplicated genes. Nat Genet 40 : 676681.[CrossRef] [PubMed]
149. Desai MM,, Fisher DS,, Murray AW . 2007. The speed of evolution and maintenance of variation in asexual populations. Curr Biol 17 : 385394.[CrossRef]
150. Gerrish PJ,, Lenski RE . 1998. The fate of competing beneficial mutations in an asexual population. Genetica 102-103 : 127144.[CrossRef]
151. Zeyl C,, DeVisser JA . 2001. Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae . Genetics 157 : 5361.[PubMed]
152. Otto SP,, Yong P . 2002. The evolution of gene duplicates. Adv Genet 46 : 451483.[CrossRef]
153. Zeyl C . 2005. The number of mutations selected during adaptation in a laboratory population of Saccharomyces cerevisiae . Genetics 169 : 18251831.[CrossRef]
154. Adams J,, Hansche PE . 1974. Population studies in microorganisms. I. Evolution of diploidy in Saccharomyces cerevisiae . Genetics 76 : 327338.[PubMed]
155. Gerstein AC,, Otto SP . 2009. Ploidy and the causes of genomic evolution. J Hered 100 : 571581.[CrossRef] [PubMed]
156. Korona R . 1999. Unpredictable fitness transitions between haploid and diploid strains of the genetically loaded yeast Saccharomyces cerevisiae . Genetics 151 : 7785.[PubMed]
157. Orr HA,, Otto SP . 1994. Does diploidy increase the rate of adaptation? Genetics 136 : 14751480.[PubMed]
158. Anderson JB,, Sirjusingh C,, Ricker N . 2004. Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae . Genetics 168 : 19151923.[CrossRef]
159. Gerstein AC . 2013. Mutational effects depend on ploidy level: all else is not equal. Biol Lett 9 : 20120614.[CrossRef] [PubMed]
160. Sellis D,, Callahan BJ,, Petrov DA,, Messer PW . 2011. Heterozygote advantage as a natural consequence of adaptation in diploids. Proc Natl Acad Sci USA 108 : 2066620671.[CrossRef]
161. Sellis D,, Kvitek DJ,, Dunn B,, Sherlock G,, Petrov DA . 2016. Heterozygote advantage is a common outcome of adaptation in Saccharomyces cerevisiae . Genetics 203 : 14011413.[CrossRef]
162. Barrett TB,, Sampson P,, Owens GK,, Schwartz SM,, Benditt EP . 1983. Polyploid nuclei in human artery wall smooth muscle cells. Proc Natl Acad Sci USA 80 : 882885.[CrossRef]
163. Reid BJ,, Blount PL,, Rubin CE,, Levine DS,, Haggitt RC,, Rabinovitch PS . 1992. Flow-cytometric and histological progression to malignancy in Barrett’s esophagus: prospective endoscopic surveillance of a cohort. Gastroenterology 102 : 12121219.[CrossRef]
164. Olaharski AJ,, Sotelo R,, Solorza-Luna G,, Gonsebatt ME,, Guzman P,, Mohar A,, Eastmond DA . 2006. Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 27 : 337343.[CrossRef]
165. Zack TI,, Schumacher SE,, Carter SL,, Cherniack AD,, Saksena G,, Tabak B,, Lawrence MS,, Zhang CZ,, Wala J,, Mermel CH,, Sougnez C,, Gabriel SB,, Hernandez B,, Shen H,, Laird PW,, Getz G,, Meyerson M,, Beroukhim R . 2013. Pan-cancer patterns of somatic copy number alteration. Nat Genet 45 : 11341140.[CrossRef]
166. Fujiwara T,, Bandi M,, Nitta M,, Ivanova EV,, Bronson RT,, Pellman D . 2005. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437 : 10431047.[CrossRef]
167. Carter SL,, Cibulskis K,, Helman E,, McKenna A,, Shen H,, Zack T,, Laird PW,, Onofrio RC,, Winckler W,, Weir BA,, Beroukhim R,, Pellman D,, Levine DA,, Lander ES,, Meyerson M,, Getz G . 2012. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol 30 : 413421.[CrossRef]
168. Brodeur GM,, Williams DL,, Look AT,, Bowman WP,, Kalwinsky DK . 1981. Near-haploid acute lymphoblastic leukemia: a unique subgroup with a poor prognosis? Blood 58 : 1419.[PubMed]
169. Farabegoli F,, Santini D,, Ceccarelli C,, Taffurelli M,, Marrano D,, Baldini N . 2001. Clone heterogeneity in diploid and aneuploid breast carcinomas as detected by FISH. Cytometry 46 : 5056.[CrossRef] [PubMed]
170. Torres L,, Ribeiro FR,, Pandis N,, Andersen JA,, Heim S,, Teixeira MR . 2007. Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases. Breast Cancer Res Treat 102 : 143155.[CrossRef]
171. Navin N,, Kendall J,, Troge J,, Andrews P,, Rodgers L,, McIndoo J,, Cook K,, Stepansky A,, Levy D,, Esposito D,, Muthuswamy L,, Krasnitz A,, McCombie WR,, Hicks J,, Wigler M . 2011. Tumour evolution inferred by single-cell sequencing. Nature 472 : 9094.[CrossRef]

Tables

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Table 1

Summary of experimental evolution studies in fungi and the ploidy and aneuploidy associated with different environmental stresses. Ploidy levels of haploid (1N), diploid (2N), triploid (3N), and tetraploid (4N) are euploid states, while aneuploidy is indicated if known.

Citation: Todd R, Forche A, Selmecki A. 2017. Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution, p 599-618. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0051-2016

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