Polyploidy in fungi: Evolution after whole-genome duplication

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1738, 2012, Pages 2497-2509

  Albertin, Warren ^a,b,c,d   Marullo, Philippe ^b,c,e  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c CEMAGREF   (France)

^d Bordeaux Sciences Agro   (France)

^e SARCO LAFFORT Group   (France)

Author keywords

Hybridization; Palaeopolyploid; Polyploid; Reticulate evolution; Whole genome duplication

Indexed keywords

ANIMALIA; EUKARYOTA; FUNGI; SACCHAROMYCES;

FUNGAL GENOME; FUNGUS; GENE DUPLICATION; GENETICS; MOLECULAR EVOLUTION; POLYPLOIDY; REVIEW; SACCHAROMYCES CEREVISIAE;

EVOLUTION, MOLECULAR; FUNGI; GENE DUPLICATION; GENOME, FUNGAL; POLYPLOIDY; SACCHAROMYCES CEREVISIAE;

EID: 84987728127     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0434     Document Type: Review

References (152)

1. Wendel, J. F. 2000 Genome evolution in polyploids. Plant Mol. Biol. 42, 225–249. (doi:10.1023/A:1006 392424384)
2. Otto, S. P. & Whitton, J. 2000 Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437. (doi:10.1146/annurev.genet.34.1.401)
3. U, N. 1935 Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot. 7, 389–452.
4. Blanc, G. & Wolfe, K. H. 2004 Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell. 16, 1667–1678. (doi:10.1105/tpc.021345)
5. Ohno, S. 1970 Evolution by gene duplication. Berlin, Germany: Springer.
6. Soltis, D. E. et al. 2009 Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348. (doi:10.3732/ajb.0800079)
7. Wolfe, K. H. & Shields, D. C. 1997 Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713. (doi:10.1038/42711)
8. Stebbins, G. L. 1950 Variation and evolution in plants, pp. 251–379. New York, NY: Columbia University Press.
9. Olive, L. S. 1953 The structure and behavior of fungus nuclei. Bot. Rev. 19, 439–586. (doi:10.1007/BF02861808)
10. Rogers, J. D. 1973 Polyploidy in fungi. Evolution 27, 153–160. (doi:10.2307/2407129)
11. Burnett, J. H. 2003 Fungal populations and species, pp. 182–184. Oxford, UK: Oxford University Press.
12. Storchova, Z. & Pellman, D. 2004 From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 5, 45–54. (doi:10.1038/Nrm1276)
13. Thorpe, P. H., Gonzalez-Barrera, S. & Rothstein, R. 2007 More is not always better: the genetic constraints of polyploidy. Trends Genet. 23, 263–266. (doi:10.1016/j.tig.2007.03.016)
14. Querol, A. & Bond, U. 2009 The complex and dynamic genomes of industrial yeasts. FEMS Microbiol. Lett. 293, 1–10. (doi:10.1111/j.1574-6968.2008.01480.x)
15. Hahn-Hagerdal, B., Wahlbom, C. F., Gardonyi, M., van Zyl, W. H., Cordero Otero, R. R. & Jonsson, L. J. 2001 Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv. Biochem. Eng. Biotechnol. 73, 53–84. (doi:10.1186/1475-2859-7-36)
16. Aguileta, G., Hood, M. E., Refregier, G. & Giraud, T. 2009 Genome evolution in plant pathogenic and symbiotic fungi. Adv. Bot. Res. 49, 151–193. (doi:10.1016/S0065-2296(08)00603-4)
17. Aury, J. M. et al. 2006 Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171–178. (doi:10.1038/nature05230)
18. Phan, I. Q., Pilbout, S. F., Fleischmann, W. & Bairoch, A. 2003 NEWT, a new taxonomy portal. Nucleic Acids Res. 31, 3822–3823. (doi:10.1093/nar/gkg516)
19. Hibbett, D. S. et al. 2007 A higher-level phylogenetic classification of the fungi. Mycol. Res. 111(Pt 5), 509–547. (doi:10.1016/j.mycres.2007.03.004)
20. Ma, L.-J. et al. 2009 Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet. 5, e1000549. (doi:10.1371/journal.pgen.1000549)
21. Emerson, R. & Wilson, C. M. 1954 Interspecific hybrids and the cytogenetics and cytotaxonomy of Euallomyces. Mycologia 46, 393–434.
22. Pawlowska, T. E. & Taylor, J. W. 2004 Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427, 733–737. (doi:10.1038/nature02290)
23. Lu, B. 1964 Polyploidy in the Basidiomycete Cyathus stercoreus. Am. J. Bot. 51, 343–347. (doi:10.2307/2440307)
24. Nielsen, K. & Yohalem, D. Y. 2001 Origin of a polyploid botrytis pathogen through interspecific hybridization between Botrytis aclada and B. byssoidea. Mycologia 93, 1064–1071. (doi:10.2307/3761668)
25. Gordon, J. L. & Wolfe, K. H. 2008 Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981. Yeast 25, 449–456. (doi:10.1002/yea.1598)
26. Meussdoerffer, F. G. 2009 A comprehensive history of beer brewing. In Handbook of brewing: processes, technology, markets (ed. H. M. Eßlinger), pp. 1–42. Weinheim, Germany: Wiley-VCH.
27. Cavalieri, D., McGovern, P. E., Hartl, D. L., Mortimer, R. & Polsinelli, M. 2003 Evidence for S. cerevisiae fermentation in ancient wine. J. Mol. Evol. 57 (Suppl 1), S226–S232. (doi:10.1007/s00239-003-0031-2)
28. Samuel, D. 1996 Investigation of ancient Egyptian baking and brewing methods by correlative microscopy. Science 273, 488–490. (doi:10.1126/science.273.5274.488)
29. Goffeau, A. et al. 1996 Life with 6000 genes. Science 274, 546, 563–547. (doi:10.1126/science.274.5287.546)
30. Smith, M. M. 1987 Molecular evolution of the Saccharomyces cerevisiae histone gene loci. J. Mol. Evol. 24, 252–259. (doi:10.1007/BF02111238)
31. Wolfe, K. H. 2001 Yesterday’s polyploids and the mystery of diploidization. Nat. Rev. Genet. 2, 333–341. (doi:10.1038/35072009)
32. Naumov, G. I., Naumova, E. S., Masneuf, I., Aigle, M., Kondratieva, V. I. & Dubourdieu, D. 2000 Natural polyploidization of some cultured yeast Saccharomyces sensu stricto: auto- and allotetraploidy. Syst. Appl. Microbiol. 23, 442–449. (doi:10.1016/S0723-2020(00)80076-4)
33. 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, 2157–2170. (doi:10.1111/j.1420-9101.2009.01828.x)
34. Al Safadi, R., Weiss-Gayet, M., Briolay, J. & Aigle, M. 2010 A polyploid population of Saccharomyces cerevisiae with separate sexes (dioecy). FEMS Yeast Res. 10, 757–768. (doi:10.1111/j.1567-1364.2010.00660.x)
35. Naumov, G. I., Naumova, E. S., Antunovics, Z. & Sipiczki, M. 2002 Saccharomyces bayanus var. uvarum in Tokaj wine-making of Slovakia and Hungary. Appl. Microbiol. Biotechnol. 59, 727–730. (doi:10.1007/s00253-002-1077-6)
36. Guijo, S., Mauricio, J. C., Salmon, J. M. & Ortega, J. M. 1997 Determination of the relative ploidy in different Saccharomyces cerevisiae strains used for fermentation and ‘flor’ film ageing of dry sherry-type wines. Yeast 13, 101–117. (doi:10.1002/(SICI)1097-0061(199702)13:2<101::AID-YEA66>3.0.CO;2-H)
37. Nilsson-Tillgren, T., Gjermansen, C., Kielland-Brandt, M., Petersen, J. & Holmberg, S. 1981 Genetic differences between Saccharomyces carlsbergensis and S. cerevisiae. Analysis of chromosome III by single chromosome transfer. Carlsberg Res. Commun. 46, 65–76. (doi:10. 1007/bf02906199)
38. Pedersen, M. 1986 DNA sequence polymorphisms in the genus Saccharomyces IV. Homoeologous chromosomes III of Saccharomyces bayanus, S. carlsbergensis, and S. uvarum. Carlsberg Res. Commun. 51, 185–202. (doi:10.1007/bf02907323)
39. Casaregola, S., Nguyen, H. V., Lapathitis, G., Kotyk, A. & Gaillardin, C. 2001 Analysis of the constitution of the beer yeast genome by PCR, sequencing and subtelomeric sequence hybridization. Int. J. Syst. Evol. Microbiol. 51, 1607–1618.
40. Dunn, B. & Sherlock, G. 2008 Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res. 18, 1610–1623. (doi:10.1101/gr.076075.108)
41. Nakao, Y., Kanamori, T., Itoh, T., Kodama, Y., Rainieri, S., Nakamura, N., Shimonaga, T., Hattori, M. & Ashikari, T. 2009 Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Res. 16, 115–129. (doi:10.1093/dnares/dsp003)
42. Libkind, D., Hittinger, C. T., Valerio, E., Goncalves, C., Dover, J., Johnston, M., Goncalves, P. & Sampaio, J. P. 2011 Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc. Natl Acad. Sci. USA 108, 14 539–14 544. (doi:10.1073/pnas.1105430108)
43. Yamada, R., Tanaka, T., Ogino, C. & Kondo, A. 2010 Gene copy number and polyploidy on products formation in yeast. Appl. Microbiol. Biotechnol. 88, 849–857. (doi:10.1007/s00253-010-2850-6)
44. Kim, H. R., Im, Y. K., Ko, H. M., Chin, J. E., Kim, I. C., Lee, H. B. & Bai, S. 2011 Raw starch fermentation to ethanol by an industrial distiller’s yeast strain of Saccharomyces cerevisiae expressing glucoamylase and α-amylase genes. Biotechnol. Lett. 33, 1643–1648. (doi:10.1007/s10529-011-0613-9)
45. Muller, L. A. & McCusker, J. H. 2009 Microsatellite analysis of genetic diversity among clinical and non-clinical Saccharomyces cerevisiae isolates suggests heterozygote advantage in clinical environments. Mol. Ecol. 18, 2779–2786. (doi:10.1111/j.1365-294X.2009. 04234.x)
46. Clemons, K. V., Park, P., McCusker, J. H., McCullough, M. J., Davis, R. W. & Stevens, D. A. 1997 Application of DNA typing methods and genetic analysis to epidemiology and taxonomy of Saccharomyces isolates. J. Clin. Microbiol. 35, 1822–1828.
47. Soltis, D. E. & Soltis, P. S. 1993 Molecular data and the dynamic nature of polyploidy. Crit. Rev. Plant Sci. 12, 243–273.
48. Chester, M., Leitch, A. R., Soltis, P. S. & Soltis, D. E. 2010 Review of the application of modern cytogenetic methods (FISH/GISH) to the study of reticulation (polyploidy/hybridisation). Genes 1, 166–192. (doi:10.3390/genes1020166)
49. Brasier, C. 2000 The rise of the hybrid fungi. Nature 405, 134–135. (doi:10.1038/35012193)
50. Collins, A., Mercado-Blanco, J., Jiménez-Diaz, R. M., Olivares, C., Clewes, E. & Barbara, D. J. 2005 Correlation of molecular markers and biological properties in Verticillium dahliae and the possible origins of some isolates. Plant Pathol. 54, 549–557. (doi:10. 1111/j.1365-3059.2005.01240.x)
51. Spiers, A. G. & Hopcroft, D. H. 1994 Comparative studies of the poplar rusts Melampsora medusae, M. larici-populina and their interspecific hybrid M.medusae-populin. Mycol. Res. 98, 889–903. (doi:10. 1016/S0953-7562(09)80260-8)
52. Newcombe, G., Stirling, B., McDonald, S. & Bradshaw Jr, H. D. 2000 Melampsora × columbiana, a natural hybrid of M. medusae and M. occidentalis. Mycol. Res. 104, 261–274. (doi:10.1017/S0953756299001665)
53. Callac, P., Jacobe de Haut, I., Imbernon, M., Guinberteau, J., Desmerger, C. & Theochari, I. 2003 A novel homothallic variety of Agaricus bisporus comprises rare tetrasporic isolates from Europe. Mycologia 95, 222–231. (doi:10.2307/3762033)
54. Hughes, K. W. & Petersen, R. H. 2001 Apparent recombination or gene conversion in the ribosomal ITS region of a Flammulina (fungi, Agaricales) hybrid. Mol. Biol. Evol. 18, 94–96. (doi:10.1093/oxfordjournals.molbev.a003724)
55. Belloch, C., Orlic, S., Barrio, E. & Querol, A. 2008 Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex. Int. J. Food Microbiol. 122, 188–195. (doi:10.1016/j.ijfoodmicro.2007.11.083)
56. Lopandic, K. et al. 2007 Genetically different wine yeasts isolated from Austrian vine-growing regions influence wine aroma differently and contain putative hybrids between Saccharomyces cerevisiae and Saccharomyces kudriavzevii. FEMS Yeast Res. 7, 953–965. (doi:10.1111/j.1567-1364.2007.00240.x)
57. Liti, G., Peruffo, A., James, S. A., Roberts, I. N. & Louis, E. J. 2005 Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex. Yeast 22, 177–192. (doi:10.1002/yea.1200)
58. Masneuf, I., Hansen, J., Groth, C., Piskur, J. & Dubourdieu, D. 1998 New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl. Environ. Microbiol. 64, 3887–3892.
59. Nguyen, H. V., Lepingle, A. & Gaillardin, C. A. 2000 Molecular typing demonstrates homogeneity of Saccharomyces uvarum strains and reveals the existence of hybrids between S. uvarum and S. cerevisiae, including the S. bayanus type strain CBS 380. Syst. Appl. Microbiol. 23, 71–85. (doi:10.1016/S0723-2020(00)80048-X)
60. Hellborg, L. & Piskur, J. 2009 Complex nature of the genome in a wine spoilage yeast, Dekkera bruxellensis. Eukaryot. Cell. 8, 1739–1749. (doi:10.1128/EC.00115-09)
61. Cappello, M. S., Poltronieri, P., Blaiotta, G. & Zacheo, G. 2010 Molecular and physiological characteristics of a grape yeast strain containing atypical genetic material. Int. J. Food. Microbiol. 144, 72–80. (doi:10.1016/j.ijfood micro.2010.08.013)
62. Foulongne-Oriol, M., Dufourcq, R., Spataro, C., Devesse, C., Broly, A., Rodier, A. & Savoie, J.-M. 2011 Comparative linkage mapping in the white button mushroom Agaricus bisporus provides foundation for breeding management. Curr. Genet. 57, 39–50. (doi:10.1007/s00294-010-0325-z)
63. Marinoni, G., Manuel, M., Petersen, R. F., Hvidtfeldt, J., Sulo, P. & Piskur, J. 1999 Horizontal transfer of genetic material among Saccharomyces yeasts. J. Bacteriol. 181, 6488–6496.
64. McCullough, J. & Herskowitz, I. 1979 Mating pheromones of Saccharomyces kluyveri: pheromone interactions between Saccharomyces kluyveri and Saccharomyces cerevisiae. J. Bacteriol. 138, 146–154.
65. Kauserud, H., Svegarden, I. B., Decock, C. & Hallenberg, N. 2007 Hybridization among cryptic species of the cellar fungus Coniophora puteana (Basidiomycota). Mol. Ecol. 16, 389–399. (doi:10.1111/j.1365-294X.2006.03129.x)
66. de Barros Lopes, M., Bellon, J. R., Shirley, N. J. & Ganter, P. F. 2002 Evidence for multiple interspecific hybridization in Saccharomyces sensu stricto species. FEMS Yeast Res. 1, 323–331. (doi:10.1016/S1567-1356(01)00051-4)
67. Muller, L. A. & McCusker, J. H. 2009 A multispecies-based taxonomic microarray reveals interspecies hybridization and introgression in Saccharomyces cerevisiae. FEMS Yeast Res. 9, 143–152. (doi:10.1111/j.1567-1364.2008.00464.x)
68. Antunovics, Z., Nguyen, H. V., Gaillardin, C. & Sipiczki, M. 2005 Gradual genome stabilisation by progressive reduction of the Saccharomyces uvarum genome in an interspecific hybrid with Saccharomyces cerevisiae. FEMS Yeast Res. 5, 1141–1150. (doi:10.1016/j.femsyr.2005.04.008)
69. Baack, E. J., Whitney, K. D. & Rieseberg, L. H. 2005 Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol. 167, 623–630. (doi:10.1111/j.1469-8137.2005.01433.x)
70. Mallet, J. 2005 Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237. (doi:10.1016/j.tree.2005.02.010)
71. Greig, D., Louis, E. J., Borts, R. H. & Travisano, M. 2002 Hybrid speciation in experimental populations of yeast. Science 298, 1773–1775. (doi:10.1126/science.1076374)
72. Devier, B., Aguileta, G., Hood, M. E. & Giraud, T. 2010 Using phylogenies of pheromone receptor genes in the Microbotryum violaceum species complex to investigate possible speciation by hybridization. Mycologia 102, 689–696. (doi:10.3852/09-192)
73. Doyle, J. J., Doyle, J. L., Rauscher, J. T. & Brown, A. H. D. 2003 Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytol. 161, 121–132. (doi:10.1046/j.1469-8137.2003.00949.x)
74. Dufresne, F. & Hebert, P. D. N. 1994 Hybridization and origins of polyploidy. Proc. R. Soc. Lond. B 258, 141–146. (doi:10.1098/rspb.1994.0154)
75. Gregory, T. R., Nicol, J. A., Tamm, H., Kullman, B., Kullman, K., Leitch, I. J., Murray, B. G., Kapraun, D. F., Greilhuber, J. & Bennett, M. D. 2007 Eukaryotic genome size databases. Nucleic Acids Research 35, D332–D338. (doi:10.1093/nar/gkl828)
76. Zaragoza, O., Garcia-Rodas, R., Nosanchuk, J. D., Cuenca-Estrella, M., Rodriguez-Tudela, J. L. & Casadevall, A. 2010 Fungal cell gigantism during mammalian infection. PLoS Pathog. 6, e1000945. (doi:10.1371/journal.ppat.1000945)
77. Hull, C. M., Raisner, R. M. & Johnson, A. D. 2000 Evidence for mating of the ‘asexual’ yeast Candida albicans in a mammalian host. Science 289, 307–310. (doi:10.1126/science.289.5477.307)
78. Bennett, R. J. & Johnson, A. D. 2003 Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 22, 2505–2515. (doi:10.1093/emboj/cdg235)
79. Ibrahim, A. S., Magee, B. B., Sheppard, D. C., Yang, M., Kauffman, S., Becker, J., Edwards Jr, J. E. & Magee, P. T. 2005 Effects of ploidy and mating type on virulence of Candida albicans. Infect. Immun. 73, 7366–7374. (doi:10.1128/IAI.73.11.7366-7374.2005)
80. Polakova, S., Blume, C., Zarate, J. A., Mentel, M., Jorck-Ramberg, D., Stenderup, J. & Piskur, J. 2009 Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc. Natl Acad. Sci. USA 106, 2688–2693. (doi:10.1073/pnas.0809793106)
81. 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, 162–168. (doi:10.1007/BF00383330)
82. Dhar, R., Sagesser, R., Weikert, C., Yuan, J. & Wagner, A. 2011 Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J. Evol. Biol. 24, 1135–1153. (doi:10.1111/j.1420-9101.2011.02249.x)
83. Welker, D. L. & Williams, K. L. 1980 Mitotic arrest and chromosome doubling using thiabendazole, cambendazole, nocodazole and Ben late in the slime mould Dictyostelium discoideum. J. Gen. Microbiol. 116, 397–407. (doi:10.1099/00221287-116-2-397)
84. Ou, S. H. 1980 Pathogen variability and host resistance in rice blast disease. Annu. Rev. Phytopathol. 18, 167–187. (doi:10.1146/annurev.py.18.090180.001123)
85. Bernard, P., Hardwick, K. & Javerzat, J.-P. 1998 Fission yeast Bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J. Cell Biol. 143, 1775–1787. (doi:10.1083/jcb.143.7.1775)
86. Baum, P., Yip, C., Goetsch, L. & Byers, B. 1988 A yeast gene essential for regulation of spindle pole duplication. Mol. Cell. Biol. 8, 5386–5397. (doi:10.1128/mcb.8.12.5386)
87. Otto, S. P. 2003 In polyploids, one plus one does not equal two. Trends Ecol. Evol. 18, 431–433. (doi:10. 1016/S0169-5347(03)00213-1)
88. Comai, L. 2005 The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836–846. (doi:10.1038/nrg1711)
89. Szadkowski, E. et al. 2010 The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol. 186, 102–112. (doi:10.1111/j.1469-8137.2010.03182.x)
90. Osborn, T. C., Butrulle, D. V., Sharpe, A. G., Pickering, K. J., Parkin, I. A., Parker, J. S. & Lydiate, D. J. 2003 Detection and effects of a homeologous reciprocal transposition in Brassica napus. Genetics 165, 1569–1577.
91. Allendorf, F. W. & Danzmann, R. G. 1997 Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 145, 1083–1092.
92. Codon, A. C., Benitez, T. & Korhola, M. 1997 Chromosomal reorganization during meiosis of Saccharomyces cerevisiae baker’s yeasts. Curr. Genet. 32, 247–259. (doi:10.1007/s002940050274)
93. Loidl, J. 1995 Meiotic chromosome pairing in triploid and tetraploid Saccharomyces cerevisiae. Genetics 139, 1511–1520.
94. Trelles-Sticken, E., Loidl, J. & Scherthan, H. 2003 Increased ploidy and KAR3 and SIR3 disruption alter the dynamics of meiotic chromosomes and telomeres. J. Cell Sci. 116, 2431–2442. (doi:10.1242/jcs.00453)
95. Mayer, V. W. & Aguilera, A. 1990 High levels of chromosome instability in polyploids of Saccharomyces cerevisiae. Mutat. Res. 231, 177–186.
96. Gerstein, A. C., Chun, H. J., Grant, A. & Otto, S. P. 2006 Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet. 2, e145. (doi:10.1371/journal.pgen.0020145)
97. Gerstein, A. C., McBride, R. M. & Otto, S. P. 2008 Ploidy reduction in Saccharomyces cerevisiae. Biol. Lett. 4, 91–94. (doi:10.1098/rsbl.2007.0476)
98. Gordon, J. L., Byrne, K. P. & Wolfe, K. H. 2011 Mechanisms of chromosome number evolution in yeast. PLoS Genet. 7, e1002190. (doi:10.1371/journal.pgen.1002190)
99. Usher, J. & Bond, U. 2009 Recombination between homoeologous chromosomes of lager yeasts leads to loss of function of the hybrid GPH1 gene. Appl. Environ. Microbiol. 75, 4573–4579. (doi:10.1128/AEM.00351-09)
100. Hanson, R. E., Islam-Faridi, M. N., Crane, C. F., Zwick, M. S., Czeschin, D. G., Wendel, J. F., McKnight, T. D., Price, H. J. & Stelly, D. M. 2000 Ty1-copia-retrotransposon behavior in a polyploid cotton. Chromosome Res. 8, 73–76. (doi:10.1023/A:1009239522541)
101. Liu, D., You, C., Liu, S., Liu, L., Duan, W., Chen, S., Yan, J. & Liu, Y. 2009 Characterization of a novel Tc1-like transposon from bream (Cyprinidae, Megalobrama) and its genetic variation in the polyploidy progeny of bream–red crucian carp crosses. J. Mol. Evol. 69, 395–403. (doi:10.1007/s00239-009-9295-5)
102. Kim, J. M., Vanguri, S., Boeke, J. D., Gabriel, A. & Voytas, D. F. 1998 Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8, 464–478.
103. Fischer, G., James, S. A., Roberts, I. N., Oliver, S. G. & Louis, E. J. 2000 Chromosomal evolution in Saccharomyces. Nature 405, 451–454. (doi:10.1038/35013058)
104. Wendel, J. F., Schnabel, A. & Seelanan, T. 1995 Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl Acad. Sci. USA 92, 280–284. (doi:10.1073/pnas.92.1.280)
105. Joly, S., Rauscher, J. T., Sherman-Broyles, S. L., Brown, A. H. & Doyle, J. J. 2004 Evolutionary dynamics and preferential expression of homeologous 18S-5.8S-26S nuclear ribosomal genes in natural and artificial glycine allopolyploids. Mol. Biol. Evol. 21, 1409–1421. (doi:10.1093/molbev/msh140)
106. Gromicho, M., Coutanceau, J.-P., Ozouf-Costaz, C. & Collares-Pereira, M. 2006 Contrast between extensive variation of 28S rDNA and stability of 5S rDNA and telomeric repeats in the diploid-polyploid Squalius alburnoides complex and in its maternal ancestor Squalius pyrenaicus (Teleostei, Cyprinidae). Chromosome Res. 14, 297–306. (doi:10.1007/s10577-006-1047-4)
107. Liti, G. & Louis, E. J. 2005 Yeast evolution and comparative genomics. Annu. Rev. Microbiol. 59, 135–153. (doi:10.1146/annurev.micro.59.030804.121400)
108. James, T. C., Usher, J., Campbell, S. & Bond, U. 2008 Lager yeasts possess dynamic genomes that undergo rearrangements and gene amplification in response to stress. Curr. Genet. 53, 139–152. (doi:10.1007/s00294-007-0172-8)
109. Kashkush, K., Feldman, M. & Levy, A. A. 2002 Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160, 1651–1659.
110. Brunet, F. d. R. G., Crollius, H. R., Paris, M., Aury, J.-M., Gibert, P., Jaillon, O., Laudet, V. & Robinson-Rechavi, M. 2006 Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol. Biol. Evol. 23, 1808–1816. (doi:10.1093/molbev/msl049)
111. LangkjAer, R. B., Cliften, P. F., Johnston, M. & Piskur, J. 2003 Yeast genome duplication was followed by asynchronous differentiation of duplicated genes. Nature 421, 848–852. (doi:10.1038/nature01419)
112. Scannell, D. R., Byrne, K. P., Gordon, J. L., Wong, S. & Wolfe, K. H. 2006 Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440, 341–345. (doi:10.1038/nature04562)
113. Bond, U., Neal, C., Donnelly, D. & James, T. C. 2004 Aneuploidy and copy number breakpoints in the genome of lager yeasts mapped by microarray hybridisation. Curr. Genet. 45, 360–370. (doi:10.1007/s00294-004-0504-x)
114. Maclean, C. J. & Greig, D. 2011 Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast. Evolution 65, 932–945. (doi:10.1111/j.1558-5646.2010.01171.x)
115. Galitski, T., Saldanha, A. J., Styles, C. A., Lander, E. S. & Fink, G. R. 1999 Ploidy regulation of gene expression. Science 285, 251–254. (doi:10.1126/science.285.5425.251)
116. Wu, C. Y., Rolfe, P. A., Gifford, D. K. & Fink, G. R. 2011 Control of transcription by cell size. PLoS Biol. 8, e1000523. (doi:10.1371/journal.pbio.1000523)
117. Parisod, C., Holderegger, R. & Brochmann, C. 2010 Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17. (doi:10.1111/j.1469-8137.2009.03142.x)
118. Albertin, W., Brabant, P., Catrice, O., Eber, F., Jenczewski, E., Chevre, A. M. & Thiellement, H. 2005 Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5, 2131–2139. (doi:10.1002/pmic. 200401092)
119. Minato, T., Yoshida, S., Ishiguro, T., Shimada, E., Mizutani, S., Kobayashi, O. & Yoshimoto, H. 2009 Expression profiling of the bottom fermenting yeast Saccharomyces pastorianus orthologous genes using oli-gonucleotide microarrays. Yeast 26, 147–165. (doi:10.1002/yea.1654)
120. Adams, K. L., Cronn, R., Percifield, R. & Wendel, J. F. 2003 Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl Acad. Sci. USA 100, 4649–4654. (doi:10.1073/pnas.0630618100)
121. Birchler, J. A., Riddle, N. C., Auger, D. L. & Veitia, R. A. 2005 Dosage balance in gene regulation: biological implications. Trends Genet. 21, 219–226. (doi:10.1016/j.tig.2005.02.010)
122. Madlung, A., Masuelli, R. W., Watson, B., Reynolds, S. H., Davison, J. & Comai, L. 2002 Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol. 129, 733–746. (doi:10.1104/pp.003095)
123. Salmon, A., Ainouche, M. L. & Wendel, J. F. 2005 Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol. Ecol. 14, 1163–1175. (doi:10.1111/j.1365-294X.2005.02488.x)
124. Yaakov, B. & Kashkush, K. 2011 Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54, 42–49. (doi:10.1139/G10-091)
125. Kraitshtein, Z., Yaakov, B., Khasdan, V. & Kashkush, K. 2010 Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186, 801–812. (doi:10.1534/genetics.110.120790)
126. Parisod, C., Salmon, A., Zerjal, T., Tenaillon, M., Grandbastien, M. A. & Ainouche, M. 2009 Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol. 184, 1003–1015. (doi:10.1111/j.1469-8137.2009.03029.x)
127. Kenan-Eichler, M., Leshkowitz, D., Tal, L., Noor, E., Melamed-Bessudo, C., Feldman, M. & Levy, A. A. 2011 Wheat hybridization and polyploidization results in deregulation of small RNas. Genetics 188, 263–272. (doi:10.1534/genetics.111.128348)
128. Colot, V. & Rossignol, J. L. 1999 Eukaryotic DNA methylation as an evolutionary device. Bioessays 21, 402–411. (doi:10.1002/(SICI)1521-1878(199905)21:5<402::AID-BIES7>3.0.CO;2-B)
129. Halme, A., Bumgarner, S., Styles, C. & Fink, G. R. 2004 Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116, 405–415. (doi:10.1016/S0092-8674(04)00118-7)
130. Querol, A., Fernandez-Espinar, M. T., del Olmo, M. & Barrio, E. 2003 Adaptive evolution of wine yeast. Int. J. Food Microbiol. 86, 3–10. (doi:10.1016/S0168-1605(03)00244-7)
131. Salmon, J.-M. 1997 Enological fermentation kinetics of an isogenic ploidy series derived from an industrial Saccharomyces cerevisiae strain. J. Biosci. Bioeng. 83, 253–260.
132. Townsend, G. F. & Lindegren, C. C. 1954 Characteristic growth patterns of the different members of a polyploid series of Saccharomyces. J. Bacteriol. 67, 480–483.
133. Lamprecht, I., Schaarschmidt, B. & Welge, G. 1976 Microcalorimetric investigation of the metabolism of yeasts. V. Influence of ploidy on growth and metabolism. Radiat. Environ. Biophys. 13, 57–61. (doi:10.1007/BF01323624)
134. Pope, G. A. et al. 2007 Metabolic footprinting as a tool for discriminating between brewing yeasts. Yeast 24, 667–679. (doi:10.1002/yea.1499)
135. Kosikov, K. V. & Raevskaia, O. G. 1976 Biological productivity of hybrids and strains of yeast cultures of different ploidy. Mikrobiologiia 45, 1040–1044.
136. Lidzbarsky, G. A., Shkolnik, T. & Nevo, E. 2009 Adaptive response to DNA-damaging agents in natural Saccharomyces cerevisiae populations from ‘Evolution Canyon’, Mt. Carmel, Israel. PLoS ONE 4, e5914. (doi:10.1371/journal.pone.0005914)
137. Conant, G. C. & Wolfe, K.H. 2007 Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol. Syst. Biol. 3, 129. (doi:10.1038/msb4100170)
138. van Hoek, M. J. & Hogeweg, P. 2009 Metabolic adaptation after whole genome duplication. Mol. Biol. Evol. 26, 2441–2453. (doi:10.1093/molbev/msp160)
139. Pavelka, N., Rancati, G., Zhu, J., Bradford, W. D., Saraf, A., Florens, L., Sanderson, B. W., Hattem, G. L. & Li, R. 2010 Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468, 321–325. (doi:10.1038/nature09529)
140. Conant, G. C. & Wolfe, K. H. 2006 Functional partitioning of yeast co-expression networks after genome duplication. PLoS Biol. 4, e109. (doi:10.1371/journal.pbio.0040109)
141. Blank, L., Kuepfer, L. & Sauer, U. 2005 Large-scale 13C-flux analysis reveals mechanistic principles of metabolic network robustness to null mutations in yeast. Genome Biol. 6, R49. (doi:10.1186/gb-2005-6-6-r49)
142. Mayrose, I., Barker, M. S. & Otto, S. P. 2010 Probabilistic models of chromosome number evolution and the inference of polyploidy. Syst. Biol. 59, 132–144. (doi:10.1093/sysbio/syp083)
143. Takagi, A., Harashima, S. & Oshima, Y. 1985 Hybridization and polyploidization of Saccharomyces cerevisiae strains by transformation-associated cell fusion. Appl. Environ. Microbiol. 49, 244–246.
144. Greig, D., Borts, R. H., Louis, E. J. & Travisano, M. 2002 Epistasis and hybrid sterility in Saccharomyces. Proc. R. Soc. Lond. B 269, 1167–1171. (doi:10.1098/rspb.2002.1989)
145. Andalis, A. A., Storchova, Z., Styles, C., Galitski, T., Pellman, D. & Fink, G. R. 2004 Defects arising from whole-genome duplications in Saccharomyces cerevisiae. Genetics 167, 1109–1121. (doi:10.1534/genetics.104.029256)
146. Song, K., Lu, P., Tang, K. & Osborn, T. C. 1995 Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl Acad. Sci. USA 92, 7719–7723. (doi:10.1073/pnas.92.17.7719)
147. Michaelis, P. 1954 Cytoplasmic inheritance in Epilobium and its theoretical significance. Adv. Genet. 6, 287–401. (doi:10.1016/S0065-2660(08)60132-7)
148. Leitch, A., Lim, K. A. R., Skalicka, K., Kovarik, A., Cigna, A. & Durante, M. 2006 Nuclear cytoplasmic interaction hypothesis and the role of translocations in Nicotiana allopolyploids. In Radiation risk estimates in normal and emergency situations (eds A. A. Cigna & M. Durante), pp. 319–326. Dordrecht, The Netherlands: Springer.
149. Lee, H.-Y., Chou, J.-Y., Cheong, L., Chang, N.-H., Yang, S.-Y. & Leu, J.-Y. 2008 Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073. (doi:10.1016/j.cell.2008.10.047)
150. Ainouche, M. L., Baumel, A., Salmon, A. & Yannic, G. 2003 Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol. 161, 165–172. (doi:10.1046/j.1469-8137.2003.00926.x)
151. Evans, B. J., Kelley, D. B., Tinsley, R. C., Melnick, D. J. & Cannatella, D. C. 2004 A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol. Phylogenet. Evol. 33, 197–213. (doi:10.1016/j.ympev.2004.04.018)
152. Grivet, L., D’Hont, A., Roques, D., Feldmann, P., Lanaud, C. & Glaszmann, J. C. 1996 RFLP mapping in cultivated sugarcane (Saccharum spp.): genome organization in a highly polyploid and aneuploid interspecific hybrid. Genetics 142, 987–1000.