Diversification at transcription factor binding sites within a species and the implications for environmental adaptation

Molecular Biology and Evolution

Volumn 28, Issue 12, 2011, Pages 3331-3344

  Ames, Ryan M ^a   Lovell, Simon C ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

evolutionary adaptation; gene duplication; gene regulation; transcription factor binding sites

Indexed keywords

TRANSCRIPTION FACTOR;

ALLELE; ARTICLE; BINDING SITE; EVOLUTIONARY ADAPTATION; FUNGAL GENE; FUNGAL STRAIN; GENE DUPLICATION; GENE SEQUENCE; NONHUMAN; PROMOTER REGION; SACCHAROMYCES;

ADAPTATION, BIOLOGICAL; BASE SEQUENCE; BINDING SITES; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENES, FUNGAL; GENETIC VARIATION; GENOME, FUNGAL; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES;

EID: 81855211086     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr167     Document Type: Article

References (55)

1. Ames RM, Rash BM, Hentges KE, Robertson DL, Delneri D, Lovell SC. 2010. Gene duplication and environmental adaptation within yeast populations. Genome Biol Evol. 2:591-601.
2. Ashburner M, Ball C, Blake J, et al. (11 co-authors). 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 25:25-29. (Pubitemid 30257031)
3. Beck T, Hall M. 1999. The tor signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689-692. (Pubitemid 129516342)
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach tomultiple testing. J R Stat Soc B Methodol. 57:289-300.
5. Blinder D, Magasanik B. 1995. Recognition of nitrogen-responsive upstream activation sequences of Saccharomyces cerevisiae by the product of the gln3 gene. J Bacteriol. 177:4190-4193.
6. Boorstein W, Craig E. 1990. Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J Biol Chem. 265:18912-18921.
7. BoorsteinW, Ziegelhoffer T, Craig E. 1994. Molecular evolution of the HSP70 multigene family. J Mol Evol. 38:1-17. (Pubitemid 24018361)
8. Carroll SB. 2005. Evolution at two levels: on genes and form. PLoS Biol . 3:1159-1166. (Pubitemid 41032181)
9. Decottignies A, Evain A, Ghislain M. 2004. Binding of Cdc48p to a ubiquitin-related UBX domain from novel yeast proteins involved in intracellular proteolysis and sporulation. Yeast 21:127-139. (Pubitemid 38219966)
10. D'haeseleer P. 2006. What are DNA sequence motifs? Nat Biotechnol. 24:423-426.
11. Doniger S, Fay J. 2007. Frequent gain and loss of functional transcription factor binding sites. PLoS Comput Biol. 3:932-942.
12. Edgar R. 2004. MUSCLE:multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res . 32:1792-1797. (Pubitemid 38832724)
13. Felsenstein J. 1989. PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164-166.
14. Fernandes L, Rodrigues-Pousada C, Struhl K. 1997. Yap, a novel family of eight bzip proteins in Saccharomyces cerevisiae with distinct biological functions.Mol Cell Biol. 17:6982-6993. (Pubitemid 27505928)
15. Force A, Lynch M, Pickett F, Amores A, Yan Y, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545. (Pubitemid 29177561)
16. Furuchi T, Ishikawa H, Miura N, Ishizuka M, Kajiya K, Kuge S, Naganuma A. 2001. Two nuclear proteins, cin5 and ydr259c, confer resistance to cisplatin in Saccharomyces cerevisiae. Mol Pharmacol. 59:470-474. (Pubitemid 32179925)
17. Ganko E, Meyers B, Vision T. 2007. Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol. 24:2298-2309. (Pubitemid 47574728)
18. Grenson M. 1966. Multiplicity of the amino acid permeases in Saccharomyces cerevisiae: I. evidence for a specific lysine-transporting system. Biochim Biophys Acta 127:339-346.
19. Gu Z, Nicolae D, Lu H, Li W. 2002. Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet. 18:609-613. (Pubitemid 35346678)
20. Gu Z, Rifkin S, White K, Li W. 2004. Duplicate genes increase gene expression diversity within and between species. Nat Genet. 36:577-579. (Pubitemid 38715982)
21. Hakes L, Pinney J, Lovell S, Oliver S, Robertson D. 2007. All duplicates are not equal: the difference between small-scale and genome duplication. Genome Biol. 8:R209.
22. Harbison C, Gordon D, Lee T, et al. (11 co-authors). 2004. Transcriptional regulatory code of a eukaryotic genome. Nature 431:99-104. (Pubitemid 39215116)
23. Haygood R, Fedrigo O, Hanson B, Yokoyama K, Wray G. 2007. Promoter regions of many neural-and nutrition-related genes have experienced positive selection during human evolution. Nat Genet. 39:1140-1144. (Pubitemid 47340653)
24. Innan H, Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet. 11:97-108.
25. Kandror O, Bretschneider N, Kreydin E, Cavalieri D, Goldberg A. 2004. Yeast adapt to near-freezing temperatures by STRE/Msn2, 4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13:771-781. (Pubitemid 38438473)
26. Kellis M, Birren B, Lander E. 2004. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617-624. (Pubitemid 38524797)
27. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120. (Pubitemid 11166431)
28. Kohn M. 2008. Rapid sequence divergence rates in the 5 prime regulatory regions of young Drosophila melanogaster duplicate gene pairs. Genet Mol Biol. 31:575-584. (Pubitemid 351935986)
29. Kostka D, HahnMW, Pollard KS. 2010. Noncoding sequences near duplicated genes evolve rapidly. Genome Biol Evol. 2:518-33.
30. Kunz J, Loeschmann A, Deuter-Reinhard M, Hall M. 2000. FAP1, a homologue of human transcription factor NF-X1, competes with rapamycin for binding to FKBP12 in yeast. MolMicrobiol. 37:1480-1493.
31. Lawless C, Pearson R, Selley J, Smirnova J, Grant C, Ashe M, Pavitt G, Hubbard S. 2009. Upstream sequence elements direct posttranscriptional regulation of gene expression under stress conditions in yeast. BMC Genomics 10:7-27.
32. Levine M, Tjian R. 2003. Transcription regulation and animal diversity. Nature 424:147-151. (Pubitemid 36858677)
33. Liti G, Carter D, Moses A, et al. (11 co-authors). 2009. Population genomics of domestic and wild yeasts. Nature 458: 337-341.
34. LynchM, O'HelyM,Walsh B, Force A. 2001. The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789-1804. (Pubitemid 34087615)
35. Martinez-Pastor M,Marchler G, Scḧuller C,Marchler-Bauer A, Ruis H, Estruch F. 1996. The Saccharomyces cerevisiae zinc finger proteinsMsn2p andMsn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15:2227-2235. (Pubitemid 26141139)
36. Ohno S. 1970. Evolution by gene duplication. New York: Springer.
37. Papp B, Ṕal C, Hurst L. 2003. Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet. 19:417-422. (Pubitemid 36930023)
38. Park C, Makova K. 2009. Coding region structural heterogeneity and turnover of transcription start sites contribute to divergence in expression between duplicate genes. Genome Biol . 10:R10.
39. Prince V, Pickett F. 2002. Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet . 3:827-837. (Pubitemid 35303515)
40. Quan X, Rassadi R, Rabie B,Matusiewicz N, StochajU. 2004. Regulated nuclear accumulation of the yeast hsp70 Ssa4p in ethanol-stressed cells is mediated by the N-terminal domain, requires the nuclear carrier Nmd5p and protein kinase C. FASEB J . NA:309471.
41. RockmanM, Hahn M, Soranzo N, Goldstein D, Wray G. 2003. Positive selectiononahuman-specific transcription factor binding site regulating IL4 expression. Curr Biol . 13:2118-2123. (Pubitemid 37502530)
42. Rouillon A, Surdin-Kerjan Y, Thomas D. 1999. Transport of sulfonium compounds. Characterization of the s-adenosylmethionine and smethylmethioninepermeases fromthe yeast Saccharomyces cerevisiae. J Biol Chem. 274:28096-28105.
43. Sandelin A, Alkema W, Engstrom P, Wasserman W, Lenhard B. 2004. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res . 32:D91-D94. (Pubitemid 38081611)
44. Smith J, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res . 23:23-35.
45. Spofford J. 1969. Heterosis and the evolution of duplications. Am. Nat . 103:407-432.
46. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456-463. (Pubitemid 40310232)
47. Stimpson H, Lewis M, Pelham H. 2006. Transferrin receptor-like proteins control the degradation of a yeastmetal transporter. EMBO J. 25:662-672. (Pubitemid 43292429)
48. Supek F, Supekova L, Nelson H, Nelson N. 1996. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc. Natl. Acad . Sci . USA. 93:5105-5110. (Pubitemid 26162878)
49. Sychrova H, Chevallier M. 1993. Cloning and sequencing of the Saccharomyces cerevisiae gene LYP1 coding for a lysine-specific permease. Yeast 9:771-782. (Pubitemid 23228877)
50. Werner-Washburne M, Becker J, Kosic-Smithers J, Craig E. 1989. Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J Bacteriol. 171:2680-2688.
51. Werner-Washburne M, Stone D, Craig E. 1987. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae.Mol Cell Biol. 7:2568-2577.
52. WhittonO. 2000. Polyploid incidence and evolution. Annu Rev Genet . 34:401-437.
53. Wu A, Wemmie J, Edgington N, GoeblM, Guevara J,Moye-RowleyW. 1993. Yeast bzip proteins mediate pleiotropic drug and metal resistance. J Biol Chem. 268:18850-18858. (Pubitemid 23273831)
54. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591. (Pubitemid 47236688)
55. ZhangZ, Gu J, Gu X. 2004.Howmuchexpressiondivergenceafter yeast gene duplication could be explained by regulatory motif evolution? Trends Genet . 20:403-407. (Pubitemid 39094567)