Dosage compensation can buffer copynumber variation in wild yeast

eLife

Volumn 4, Issue MAY, 2015, Pages

  Hose, James ^a   Yong, Chris Mun ^a   Sardi, Maria ^a   Wang, Zhishi ^b   Newton, Michael A ^a,b   Gasch, Audrey P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Madison   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MESSENGER RNA; OXIDOREDUCTASE; TRANSCRIPTOME;

ANEUPLOIDY; ARTICLE; CELL STRUCTURE; CHROMOSOME 12; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA MICROARRAY; DOWN REGULATION; GENE AMPLIFICATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRAIT; MOLECULAR CLONING; MOLECULAR ECOLOGY; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; YEAST; BIOLOGICAL MODEL; EVOLUTION; FUNGAL GENE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; SACCHAROMYCES CEREVISIAE; STATISTICAL MODEL;

ANEUPLOIDY; BIOLOGICAL EVOLUTION; DOSAGE COMPENSATION, GENETIC; GENE DOSAGE; GENES, FUNGAL; GENETIC VARIATION; LINEAR MODELS; MODELS, GENETIC; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 84930613697     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05462     Document Type: Article

References (80)

1. Anders S, Pyl PT, Huber W. 2014. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169. doi: 10.1093/bioinformatics/btu638.
2. Antonarakis SE, Lyle R, Dermitzakis ET, Reymond A, Deutsch S. 2004. Chromosome 21 and Down syndrome: from genomics to pathophysiology. Nature Reviews 5:725-738. doi: 10.1038/nrg1448.
3. Benjamini Y, Hochberg Y. 1995. Controllign the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57:289-300.
4. Birchler JA, Veitia RA. 2007. The gene balance hypothesis: from classical genetics to modern genomics. The Plant Cell 19:395-402. doi: 10.1105/tpc.106.049338.
5. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114-2120. doi: 10.1093/bioinformatics/btu170.
6. 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. doi: 10.1186/1471-2164-9-524.
7. Chang SL, Lai HY, Tung SY, Leu JY. 2013. Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLOS Genetics 9:e1003232. doi: 10.1371/journal.pgen.1003232.
8. Chasman D, Ho YH, Berry DB, Nemec CM, MacGilvray ME, Hose J, Merrill AE, Lee MV, Will JL, Coon JJ, Ansari AZ Craven M, Gasch AP. 2014. Pathway connectivity and signaling coordination in the yeast stress-activated signaling network. Molecular Systems Biology 10:759. doi: 10.15252/msb.20145120.
9. Chen G, Bradford WD, Seidel CW, Li R. 2012. Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature 482:246-250. doi: 10.1038/nature10795.
10. Conti A, Fabbrini F, D'Agostino P, Negri R, Greco D, Genesio R, D'Armiento M, Olla C, Paladini D, Zannini M Nitsch L. 2007. Altered expression of mitochondrial and extracellular matrix genes in the heart of human fetuses with chromosome 21 trisomy. BMC Genomics 8:268. doi: 10.1186/1471-2164-8-268.
11. Dabeva MD, Warner JR. 1987. The yeast ribosomal protein L32 and its gene. The Journal of Biological Chemistry 262:16055-16059.
12. de Jong L, Elzinga SD, McCammon MT, Grivell LA, van der Spek H. 2000. Increased synthesis and decreased stability of mitochondrial translation products in yeast as a result of loss of mitochondrial (NAD(+))-dependent isocitrate dehydrogenase. FEBS Letters 483:62-66. doi: 10.1016/S0014-5793(00)02086-X.
13. De Smet R, Van de Peer Y. 2012. Redundancy and rewiring of genetic networks following genome-wide duplication events. Current Opinion in Plant Biology 15:168-176. doi: 10.1016/j.pbi.2012.01.003.
14. Dephoure N, Hwang S, O'Sullivan C, Dodgson SE, Gygi SP, Amon A, Torres EM. 2014. Quantitative proteomic analysis reveals posttranslational responses to aneuploidy in yeast. eLife e03023. doi: 10.7554/eLife.03023.
15. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics 43:491-498. doi: 10.1038/ng.806.
16. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, Botstein D. 2002. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of USA 99:16144-16149. doi: 10.1073/pnas.242624799.
17. Dunn B, Levine RP, Sherlock G. 2005. Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 6:53. doi: 10.1186/1471-2164-6-53.
18. 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 Research 22:908-924. doi: 10.1101/gr.130310.111.
19. Edi CV, Djogbenou L, Jenkins AM, Regna K, Muskavitch MA, Poupardin R, Jones CM, Essandoh J, Ketoh GK, Paine MJ, Koudou BG, Donnelly MJ, Ranson H, Weetman D. 2014. CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. PLOS Genetics 10: e1004236. doi: 10.1371/journal.pgen.1004236.
20. Elzinga SD, Bednarz AL, van Oosterum K, Dekker PJ, Grivell LA. 1993. Yeast mitochondrial NAD(+)-dependent isocitrate dehydrogenase is an RNA-binding protein. Nucleic Acids Research 21:5328-5331. doi: 10.1093/nar/21. 23.5328.
21. Fay JC, Benavides JA. 2005. Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLOS Genetics 1:66-71. doi: 10.1371/journal.pgen.0010005.
22. Fox J, Weisberg S. 2011. An R Companion to Applied Regression. 2nd edition. Thousand Oaks CA: Sage. URL: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.
23. Freschi L, Courcelles M, Thibault P, Michnick SW, Landry CR. 2011. Phosphorylation network rewiring by gene duplication. Molecular Systems Biology 7:504. doi: 10.1038/msb.2011.43.
24. Gasch AP. 2002. Yeast genomic expression studies using DNA microarrays. Methods in Enzymology 350:393-414.
25. 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 Genetics 4:e1000303. doi: 10.1371/journal.pgen.1000303.
26. Gu X, Zhang Z, Huang W. 2005. Rapid evolution of expression and regulatory divergences after yeast gene duplication. Proceedings of the National Academy of Sciences of USA 102:707-712. doi: 10.1073/pnas. 0409186102.
27. Gu Z, Rifkin SA, White KP, Li WH. 2004. Duplicate genes increase gene expression diversity within and between species. Nature Genetics 36:577-579. doi: 10.1038/ng1355.
28. Hall BG, Acar H, Nandipati A, Barlow M. 2014. Growth rates made easy. Molecular Biology and Evolution 31: 232-238. doi: 10.1093/molbev/mst187.
29. Helguera P, Seiglie J, Rodriguez J, Hanna M, Helguera G, Busciglio J. 2013. Adaptive downregulation of mitochondrial function in down syndrome. Cell Metabolism 17:132-140. doi: 10.1016/j.cmet.2012.12.005.
30. Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR, Slade D, Burchard J, Dow S, Ward TR, Kidd MJ, Friend SH Marton MJ. 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nature Genetics 25: 333-337. doi: 10.1038/77116.
31. Jaillon O, Aury JM, Wincker P. 2009. 'Changing by doubling', the impact of whole genome duplications in the evolution of eukaryotes. Comptes Rendus Biologies 332:241-253. doi: 10.1016/j.crvi.2008.07.007.
32. Koszul R, Caburet S, Dujon B, Fischer G. 2004. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. The EMBO Journal 23:234-243. doi: 10.1038/sj.emboj.7600024.
33. Kvitek DJ, Will JL, Gasch AP. 2008. Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLOS Genetics 4:e1000223. doi: 10.1371/journal.pgen.1000223.
34. Landry CR, Lemos B, Rifkin SA, Dickinson WJ, Hartl DL. 2007. Genetic properties influencing the evolvability of gene expression. Science 317:118-121. doi: 10.1126/science.1140247.
35. Leducq JB, Charron G, Samani P, Dube AK, Sylvester K, James B, Almeida P, Sampaio JP, Hittinger CT, Bell G Landry CR. 2014. Local climatic adaptation in a widespread microorganism. Proceedings. Biological Sciences/ The Royal Society 281:20132472. doi: 10.1098/rspb.2013.2472.
36. Lee MV, Topper SE, Huberl SL, Hose J, Wenger CD, Coon J, Gasch AP. 2011. A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Molecular Systems Biology 7:514. doi: 10.1038/msb. 2011.48.
37. Lewis JA, Elkon IM, McGee MA, Higbee AJ, Gasch AP. 2010. Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics 186:1197-1205. doi: 10.1534/genetics. 110.121871.
38. Lewis JA, Gasch AP. 2012. Natural variation in the yeast glucose-signaling network reveals a new role for the Mig3p transcription factor. G3 2:1607-1612. doi: 10.1534/g3.112.004127.
39. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760. doi: 10.1093/bioinformatics/btp324.
40. Li WH, Yang J, Gu X. 2005. Expression divergence between duplicate genes. Trends in Genetics 21:602-607. doi: 10.1016/j.tig.2005.08.006.
41. Lintas C, Sacco R, Persico AM. 2012. Genome-wide expression studies in autism spectrum disorder, Rett syndrome, and Down syndrome. Neurobiology of Disease 45:57-68. doi: 10.1016/j.nbd.2010.11.010.
42. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O'Kelly MJ, van Oudenaarden A, Barton DB, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ. 2009. Population genomics of domestic and wild yeasts. Nature 458:337-341. doi: 10.1038/nature07743.
43. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
44. Lynch M, O'Hely M, Walsh B, Force A. 2001. The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789-1804.
45. Makanae K, Kintaka R, Makino T, Kitano H, Moriya H. 2013. Identification of dosage-sensitive genes in Saccharomyces cerevisiae using the genetic tug-of-war method. Genome Research 23:300-311. doi: 10.1101/gr.146662.112.
46. McLachlan G, Peel D. 2000. Finite Mixture Models: Wiley Series in Probability and Statistics. New York: Wiley.
47. Mick DU, Fox TD, Rehling P. 2011. Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nature Reviews. Molecular Cell Biology 12:14-20. doi: 10.1038/nrm3029.
48. Newton MA, Noueiry A, Sarkar D, Ahlquist P. 2004. Detecting differential gene expression with a semiparametric hierarchical mixture method. Biostatistics 5:155-176. doi: 10.1093/biostatistics/5.2.155.
49. 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 Biology 11:e1001653. doi: 10.1371/journal.pbio.1001653.
50. Ohno S. 1970. Evolution by Gene Duplication. Springer-Verlag. p. 160.
51. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R. 2010. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468:321-325. doi: 10. 1038/nature09529.
52. Prandini P, Deutsch S, Lyle R, Gagnebin M, Delucinge Vivier C, Delorenzi M, Gehrig C, Descombes P, Sherman S Dagna Bricarelli F, Baldo C, Novelli A, Dallapiccola B, Antonarakis SE. 2007. Natural gene-expression variation in Down syndrome modulates the outcome of gene-dosage imbalance. American Journal of Human Genetics 81: 252-263. doi: 10.1086/519248.
53. Presser A, Elowitz MB, Kellis M, Kishony R. 2008. The evolutionary dynamics of the Saccharomyces cerevisiae protein interaction network after duplication. Proceedings of the National Academy of Sciences of USA 105: 950-954. doi: 10.1073/pnas.0707293105.
54. Pu S, Wong J, Turner B, Cho E, Wodak SJ. 2009. Up-to-date catalogues of yeast protein complexes. Nucleic Acids Research 37:825-831. doi: 10.1093/nar/gkn1005.
55. 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 135:879-893. doi: 10.1016/j.cell.2008.09.039.
56. Robinson MD, Grigull J, Mohammad N, Hughes TR. 2002. FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3:35. doi: 10.1186/1471-2105-3-35.
57. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. doi: 10.1093/bioinformatics/btp616.
58. Roper RJ, Reeves RH. 2006. Understanding the basis for Down syndrome phenotypes. PLOS Genetics 2:e50. doi: 10.1371/journal.pgen.0020050.
59. Sandegren L, Andersson DI. 2009. Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nature Reviews. Microbiology 7:578-588. doi: 10.1038/nrmicro2174.
60. Schuster-Bockler B, Conrad D, Bateman A. 2010. Dosage sensitivity shapes the evolution of copy-number varied regions. PLOS ONE 5:e9474. doi: 10.1371/journal.pone.0009474.
61. Selmecki A, Forche A, Berman J. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313:367-370. doi: 10.1126/science.1128242.
62. Sheltzer JM, Torres EM, Dunham MJ, Amon A. 2012. Transcriptional consequences of aneuploidy. Proceedings of the National Academy of Sciences of USA 109:12644-12649. doi: 10.1073/pnas.1209227109.
63. Siegel JJ, Amon A. 2012. New insights into the troubles of aneuploidy. Annual Review of Cell and Developmental Biology 28:189-214. doi: 10.1146/annurev-cellbio-101011-155807.
64. Skelly DA, Merrihew GE, Riffle M, Connelly CF, Kerr EO, Johansson M, Jaschob D, Graczyk B, Shulman NJ Wakefield J, Cooper SJ, Fields S, Noble WS, Muller EG, Davis TN, Dunham MJ, Maccoss MJ, Akey JM. 2013. Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast. Genome Research 23:1496-1504. doi: 10.1101/gr.155762.113.
65. Springer M, Weissman JS, Kirschner MW. 2010. A general lack of compensation for gene dosage in yeast. Molecular Systems Biology 6:368. doi: 10.1038/msb.2010.19.
66. Tan Z, Hays M, Cromie GA, Jeffery EW, Scott AC, Ahyong V, Sirr A, Skupin A, Dudley AM. 2013. Aneuploidy underlies a multicellular phenotypic switch. Proceedings of the National Academy of Sciences of USA 110: 12367-12372. doi: 10.1073/pnas.1301047110.
67. Torres EM, Dephoure N, Panneerselvam A, Tucker CM, Whittaker CA, Gygi SP, Dunham MJ, Amon A. 2010. Identification of aneuploidy-tolerating mutations. Cell 143:71-83. doi: 10.1016/j.cell.2010.08.038.
68. 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 317:916-924. doi: 10.1126/science.1142210.
69. Valenti D, de Bari L, De Filippis B, Henrion-Caude A, Vacca RA. 2014. Mitochondrial dysfunction as a central actor in intellectual disability-related diseases: an overview of Down syndrome, autism, Fragile X and Rett syndrome. Neuroscience and Biobehavioral Reviews. doi: 10.1016/j.neubiorev.2014.01.012.
70. Van Loon AP, Van Eijk E, Grivell LA. 1983. Biosynthesis of the ubiquinol-cytochrome c reductase complex in yeast. Discoordinate synthesis of the 11-kd subunit in response to increased gene copy number. The EMBO Journal 2: 1765-1770.
71. Vilardell J, Warner JR. 1997. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Molecular and Cellular Biology 17:1959-1965.
72. Wang RT, Ahn S, Park CC, Khan AH, Lange K, Smith DJ. 2011. Effects of genome-wide copy number variation on expression in mammalian cells. BMC Genomics 12:562. doi: 10.1186/1471-2164-12-562.
73. Wang Y, Wang X, Paterson AH. 2012. Genome and gene duplications and gene expression divergence: a view from plants. Annals of the New York Academy of Sciences 1256:1-14. doi: 10.1111/j.1749-6632.2011.06384.x.
74. Will JL, Kim HS, Clarke J, Painter JC, Fay JC, Gasch AP. 2010. Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLOS Genetics 6:e1000893. doi: 10.1371/journal. pgen.1000893.
75. Woodwark C, Bateman A. 2011. The characterisation of three types of genes that overlie copy number variable regions. PLOS ONE 6:e14814. doi: 10.1371/journal.pone.0014814.
76. Wu CY, Rolfe PA, Gifford DK, Fink GR. 2010. Control of transcription by cell size. PLOS Biology 8:e1000523. doi: 10.1371/journal.pbio.1000523.
77. 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. Proceedings of the National Academy of Sciences of USA 109:21010-21015. doi: 10.1073/pnas.1211150109.
78. Zhang Y, Malone JH, Powell SK, Periwal V, Spana E, Macalpine DM, Oliver B. 2010. Expression in aneuploid Drosophila S2 cells. PLOS Biology 8:e1000320. doi: 10.1371/journal.pbio.1000320.
79. Zhou J, Lemos B, Dopman EB, Hartl DL. 2011. Copy-number variation: the balance between gene dosage and expression in Drosophila melanogaster. Genome Biology and Evolution 3:1014-1024. doi: 10.1093/gbe/evr023.
80. Zhu YO, Siegal ML, Hall DW, Petrov DA. 2014. Precise estimates of mutation rate and spectrum in yeast. Proceedings of the National Academy of Sciences of USA 111:E2310-E2318. doi: 10.1073/pnas.1323011111.