Heterochronic meiotic misexpression in an interspecific yeast hybrid

Molecular Biology and Evolution

Volumn 31, Issue 6, 2014, Pages 1333-1342

  Swain Lenz, Devjanee ^a   Riles, Linda ^a   Fay, Justin C ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

hybrid; misexpression; speciation; yeast

Indexed keywords

CIS ACTING ELEMENT; RIBOSOME PROTEIN; TRANS ACTING FACTOR;

ARTICLE; CELL NUCLEUS; CELL POPULATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FUNGAL GENE; GENE EXPRESSION; GENE MISEXPRESSION; HETEROCHROMATIN; HYBRID GENE; INTERSPECIFIC HYBRID; INTERSPECIFIC YEAST HYBRID; MEIOSIS; NONHUMAN; RNA SEQUENCE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS; SPOROGENESIS; YEAST; YEAST CELL; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; SACCHAROMYCES; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENETIC SPECIATION; HYBRIDIZATION, GENETIC; MEIOSIS; SACCHAROMYCES; SPECIES SPECIFICITY;

EID: 84901446369     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu098     Document Type: Article

References (54)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106.
2. Artieri CG, Singh RS. 2010. Molecular evidence for increased regulatory conservation during metamorphosis, and against deleterious cascading effects of hybrid breakdown in Drosophila. BMC Biol. 8:26.
3. Bayes JJ, Malik HS. 2009. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326:1538-1541.
4. Carter D. 2008. Wellcome Trust Sanger Institute Saccharomyces Genome Resequencing Project: user manual. Cambridge (UK): The Sanger Institute. p. 1-32. Available from: ftp://ftp.sanger.ac.uk/pub/dmc/yeast/latest.
5. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, Christie KR, Costanzo MC, Dwight SS, Engel SR, et al. 2012. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 40:D700-D705.
6. Chou J-Y, Hung Y-S, Lin K-H, Lee H-Y, Leu J-Y. 2010. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 8:e1000432.
7. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I. 1998. The transcriptional program of sporulation in budding yeast. Science 282:699-705.
8. Coolon JD, Wittkopp PJ. 2013. Cis-and trans-regulation in Drosophila interspecific hybrids. In: Chen ZJ, Birchler JA, editors. Polyploid and hybrid genomics. Oxford: John Wiley, UK. p. 37-58.
9. Cubillos FA, Louis EJ, Liti G. 2009. Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Res. 9:1217-1225.
10. Dong Y, Bogdanova A, Habermann B, Zachariae W, Ahringer J. 2007. Identification of the C. elegans anaphase promoting complex subunit Cdc26 by phenotypic profiling and functional rescue in yeast. BMC Dev Biol. 7:19.
11. Emerson JJ, Hsieh LC, Sung HM, Wang TY, Huang CJ, Lu HHS, Lu MYJ, Wu SH, LiWH. 2010. Natural selection on cis and trans regulation in yeasts. Genome Res. 20:826-836.
12. Ferguson J, Gomes S, Civetta A. 2013. Rapid male-specific regulatory divergence and down regulation of spermatogenesis genes in Drosophila species hybrids. PLoS One 8:e61575.
13. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111.
14. Galbraith AM, Bullard SA, Jiao K, Nau JJ, Malone RE. 1997. Recombination and the progression of meiosis in Saccharomyces cerevisiae. Genetics 146:481-489.
15. Gonçalves P, Valério E, Correia C, de Almeida JMGCF, Sampaio JP. 2011. Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6:e20739.
16. Good JM, Giger T, Dean MD, Nachman MW. 2010. Widespread overexpression of the X chromosome in sterile F(1)hybrid mice. PLoS Genet. 6:e1001148.
17. Gould SJ. 1977. Ontogeny and phylogeny. Cambridge (MA): Harvard University Press.
18. Graze RM, McIntyre LM, Main BJ, Wayne ML, Nuzhdin SV. 2009. Regulatory divergence in Drosophila melanogaster and D. simulans, a genomewide analysis of allele-specific expression. Genetics 183: 547-561.
19. Greig D, Louis EJ, Borts RH, Travisano M. 2002. Hybrid speciation in experimental populations of yeast. Science 298:1773-1775.
20. Greig D, Travisano ME, Louis EJ, Borts RH. 2003. A role for the mismatch repair system during incipient speciation in Saccharomyces. J Evol Biol. 16:429-437.
21. Haerty W, Singh RS. 2006. Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila. Mol Biol Evol. 23:1707-1714.
22. Hunter N, Chambers SR, Louis EJ, Borts RH. 1996. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15:1726-1733.
23. Landry CR, Wittkopp PJ, Taubes CH, Ranz JM, Clark AG, Hartl DL. 2005. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171: 1813-1822.
24. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
25. 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.
26. Liti G, Barton DBH, Louis EJ. 2006. Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174: 839-850.
27. Llopart A. 2012. The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids. Mol Biol Evol. 29:3873-3886.
28. Lu X, Shapiro JA, Ting CT, Li Y, Li C, Xu J, Huang H, Cheng YJ, Greenberg AJ, Li SH, et al. 2010. Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility. Genome Res. 20:1097-1102.
29. Maheshwari S, Barbash DA. 2012. Cis-by-trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet. 8:e1002597.
30. Malone JH, Chrzanowski TH, Michalak P. 2007. Sterility and gene expression in hybrid males of Xenopus laevis and X. muelleri. PLoS One 2:e781.
31. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. 2010. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 20:816-825.
32. Michalak P, Noor MAF. 2003. Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol. 20: 1070-1076.
33. Moehring AJ, Teeter KC, Noor MAF. 2006. Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol Biol Evol. 24:137-145.
34. Murphy HA, Kuehne HA, Francis CA, Sniegowski PD. 2006. Mate choice assays and mating propensity differences in natural yeast populations. Biol Lett. 2:553-556.
35. Murphy HA, Zeyl CW. 2012. Prezygotic isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus through differences in mating speed and germination timing. Evolution 66: 1196-1209.
36. Ortíz-Barrientos D, Counterman BA, Noor MAF. 2006. Gene expression divergence and the origin of hybrid dysfunctions. Genetica 129: 71-81.
37. Parker HR, Philipp DP, Whitt GS. 1985. Gene regulatory divergence among species estimated by altered developmental patters in interspecific hybrids. Mol Biol Evol. 2:217-250.
38. Primig M, Esposito RE. 2000. The core meiotic transcriptome in budding yeasts. Nat Genet. 6:415-423.
39. Ranz JM, Namgyal K, Gibson G, Hartl DL. 2004. Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res. 14:373-379.
40. Ranz JM, Yeh S-D, Nyberg KG, Machado CA. 2013. Transcriptome profiling of Drosophila interspecific hybrids: insights into mechanisms of regulatory divergence and hybrid dysfunction. In: Chen ZJ, Birchler JA, editors. Polyploid and hybrid genomics. Oxford: John Wiley. p. 15-36.
41. Renaut S, Nolte AW, Bernatchez L. 2009. Gene expression divergence and hybrid misexpression between Lake Whitefish species pairs (Coregonus spp. Salmonidae). Mol Biol Evol. 26:925-936.
42. Rottscheidt R, Harr B. 2007. Extensive additivity of gene expression differentiates subspecies of the house mouse. Genetics 177:1553-1567.
43. Sackton TB, Montenegro H, Hartl DL, Lemos B. 2011. Interspecific Y chromosome introgressions disrupt testis-specific gene expression andmale reproductive phenotypes in Drosophila. Proc Natl Acad Sci USA. 108:17046-17051.
44. Schaefke B, Emerson JJ, Wang TY, Lu MY, Hsieh LC, Li WH. 2013. Inheritance of gene expression level and selective constraints on trans-and cis-regulatory changes in yeast. Mol Biol Evol. 30: 2121-2133.
45. Shah R, Jensen S, Frenz LM, Johnson AL, Johnston LH. 2001. The Spo12 protein of Saccharomyces cerevisiae: a regulator of mitotic exit whose cell cycle-dependent degradation is mediated by the anaphase-promoting complex. Genetics 159:965-980.
46. Simola DF, Francis C, Sniegowski PD, Kim J. 2010. Heterochronic evolution reveals modular timing changes in budding yeast transcriptomes. Genome Biol. 11:R105.
47. Somel M, Franz H, Yan Z, Lorenc A, Guo S, Giger T, Kelso J, Nickel B, Dannemann M, Bahn S, et al. 2009. Transcriptional neoteny in the human brain. Proc Natl Acad Sci USA. 106:5743-5748.
48. Sundararajan V, Civetta A. 2011. Male sex interspecies divergence and down regulation of expression of spermatogenesis genes in Drosophila sterile hybrids. J Mol Evol. 72:80-89.
49. Tirosh I, Reikhav S, Levy AA, Barkai N. 2009. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659-662.
50. True JR, Haag ES. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evol Dev. 3:109-119.
51. Tsubouchi H, Roeder GS. 2006. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 20:1766-1775.
52. Wittkopp PJ, Haerum BK, Clark AG. 2004. Evolutionary changes in cis and trans gene regulation. Nature 430:85-88.
53. Wittkopp PJ, Haerum BK, Clark AG. 2008. Independent effects of cisand trans-regulatory variation on gene expression in Drosophila melanogaster. Genetics 178:1831-1835.
54. Xu M, He X. 2011. Genetic incompatibility dampens hybrid fertility more than hybrid viability: yeast as a case study. PLoS One 6: e18341.