Rewiring of posttranscriptional RNA regulons: Puf4p in fungi as an example

Molecular Biology and Evolution

Volumn 29, Issue 9, 2012, Pages 2169-2176

  Jiang, Huifeng ^a,b   Guo, Xiaoxian ^a,c   Xu, Lin ^a   Gu, Zhenglong ^a  

^a Cornell University ^*  (United States)

^b Tianjin Airport Economic Area   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

evolution of gene regulation; posttranscriptional regulon; yeast

Indexed keywords

ARTICLE; EUKARYOTE; EVOLUTION; FUNGUS; GENE REGULATORY NETWORK; HUMAN; MITOCHONDRION; NONHUMAN; PHENOTYPE; PROTEIN PROCESSING; REGULON;

AMINO ACID SEQUENCE; CLUSTER ANALYSIS; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, MITOCHONDRIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

EUKARYOTA; FUNGI; PEZIZOMYCOTINA; SACCHAROMYCOTINA;

EID: 84865523514     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss085     Document Type: Article

References (61)

1. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 57:289-300.
2. Bockaert J, Pin JP. 1999. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J. 18:1723-1729. (Pubitemid 29158516)
3. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, Seringhaus MR, Wang LY, Gerstein M, Snyder M. 2007. Divergence of transcription factor binding sites across related yeast species. Science 317:815-819. (Pubitemid 47257921)
4. Byrne KP, Wolfe KH. 2005. The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15:1456-1461. (Pubitemid 41400914)
5. Carroll SB. 2005. Evolution at two levels: on genes and form. PLoS Biol. 3:e245.
6. Chen K, Rajewsky N. 2007. The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet. 8:93-103. (Pubitemid 46122839)
7. Chritton JJ, Wickens M. 2010. Translational repression by PUF proteins in vitro. RNA 16:1217-1225.
8. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660-663. (Pubitemid 34614826)
9. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. (Pubitemid 38832724)
10. Emerson JJ, Hsieh LC, Sung HM, Wang TY, Huang CJ, Lu HH, Lu MY, Wu SH, Li WH. 2010. Natural selection on cis and trans regulation in yeasts. Genome Res. 20:826-836.
11. Fitzpatrick DA, Logue ME, Stajich JE, Butler G. 2006. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol. 6:99.
12. Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ. 2005. Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci USA. 102:17675-17680. (Pubitemid 41803556)
13. Frankel N, Davis GK, Vargas D, Wang S, Payre F, Stern DL. 2010. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466:490-493.
14. Galgano A, Forrer M, Jaskiewicz L, Kanitz A, Zavolan M, Gerber AP. 2008. Comparative analysis of mRNA targets for human PUFfamily proteins suggests extensive interaction with the miRNA regulatory system. PLoS One. 3:e3164.
15. Gerber AP, Herschlag D, Brown PO. 2004. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2:E79.
16. Gerber AP, Luschnig S, Krasnow MA, Brown PO, Herschlag D. 2006. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci USA. 103:4487-4492.
17. Goldstrohm AC, Hook BA, Seay DJ, Wickens M. 2006. PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol. 13:533-539. (Pubitemid 43848908)
18. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Cell Biol. 24:5534-5547. (Pubitemid 38738184)
19. Hayashi M, Schilke B, Marszalek J, Williams B, Craig EA. 2011. Ancient gene duplication provided a key molecular step for anaerobic growth of Baker's yeast. Mol Biol Evol. 28:2005-2017.
20. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO. 2008. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6:e255.
21. Hook BA, Goldstrohm AC, Seay DJ, Wickens M. 2007. Two yeast PUF proteins negatively regulate a single mRNA. J Biol Chem. 282:15430-15438. (Pubitemid 47093267)
22. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. 2003. Global analysis of protein localization in budding yeast. Nature 425:686-691. (Pubitemid 37314307)
23. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, Barkai N. 2005. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309:938-940. (Pubitemid 41099931)
24. Jacob F. 1977. Evolution and tinkering. Science 196:1161-1166.
25. Jacob F. 2001. Complexity and tinkering. Ann N Y Acad Sci. 929:71-73. (Pubitemid 32386051)
26. Jiang H, Guan W, Gu Z. 2010. Tinkering evolution of posttranscriptional RNA regulons: puf3p in fungi as an example. PLoS Genet. 6:e1001030.
27. Jordan IK. 2006. Evolutionary tinkering with transposable elements. Proc Natl Acad Sci USA. 103:7941-7942. (Pubitemid 43801032)
28. Kadyrova LY, Habara Y, Lee TH, Wharton RP. 2007. Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development 134:1519-1527. (Pubitemid 46746304)
29. Kaplan T, Li XY, Sabo PJ, Thomas S, Stamatoyannopoulos JA, Biggin MD, Eisen MB. 2011. Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet. 7:e1001290.
30. Keene JD. 2007. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet. 8:533-543. (Pubitemid 46955210)
31. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science 188:107-116.
32. Kleine T, Leister D. 2007. Evolutionary tinkering: birth of a novel chloroplast protein. Biochem J. 403:e13-14.
33. Larkin MA, Blackshields G, Brown NP, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. (Pubitemid 350162903)
34. Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, Whiteway M. 2010. Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol. 8:e1000329.
35. Lee D, Ohn T, Chiang YC, Quigley G, Yao G, Liu Y, Denis CL. 2010. PUF3 acceleration of deadenylation in vivo can operate independently of CCR4 activity, possibly involving effects on the PAB1-mRNP structure. J Mol Biol. 399:562-575.
36. Lin H, Spradling AC. 1997. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124:2463-2476. (Pubitemid 27309745)
37. Long M. 2001. Evolution of novel genes. Curr Opin Genet Dev. 11:673-680. (Pubitemid 33000340)
38. Long M, Betran E, Thornton K, Wang W. 2003. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 4:865-875. (Pubitemid 37345613)
39. Long M, Langley CH. 1993. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 260:91-95. (Pubitemid 23122751)
40. Mandrioli M. 2004. Epigenetic tinkering and evolution: is there any continuity in the role of cytosine methylation from invertebrates to vertebrates? Cell Mol Life Sci. 61:2425-2427. (Pubitemid 39586506)
41. Mata J, Marguerat S, Bahler J. 2005. Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem Sci. 30:506-514. (Pubitemid 41206506)
42. Miller MT, Higgin JJ, Hall TM. 2008. Basis of altered RNA-binding specificity by PUF proteins revealed by crystal structures of yeast Puf4p. Nat Struct Mol Biol. 15:397-402. (Pubitemid 351483388)
43. Morris AR, Mukherjee N, Keene JD. 2008. Ribonomic analysis of human Pum1 reveals cis-trans conservation across species despite evolution of diverse mRNA target sets. Mol Cell Biol. 28:4093-4103. (Pubitemid 351812993)
44. Murata Y, Wharton RP. 1995. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80:747-756.
45. Prokisch H, Andreoli C, Ahting U, Heiss K, Ruepp A, Scharfe C, Meitinger T. 2006. MitoP2: the mitochondrial proteome database-now including mouse data. Nucleic Acids Res. 34:D705-711.
46. Quenault T, Lithgow T, Traven A. 2011. PUF proteins: repression, activation and mRNA localization. Trends Cell Biol. 21:104-112.
47. Remm M, Storm CE, Sonnhammer EL. 2001. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 314:1041-1052. (Pubitemid 34073068)
48. Rodriguez-Caso C, Medina MA, Sole RV. 2005. Topology, tinkering and evolution of the human transcription factor network. FEBS J. 272:6423-6434. (Pubitemid 41815629)
49. Rozpedowska E, Hellborg L, Ishchuk OP, Orhan F, Galafassi S, Merico A, Woolfit M, Compagno C, Piskur J. 2011. Parallel evolution of the make-accumulate-consume strategy in Saccharomyces and Dekkera yeasts. Nat Commun. 2:302.
50. Shou C, Bhardwaj N, Lam HY, Yan KK, Kim PM, Snyder M, Gerstein MB. 2011. Measuring the evolutionary rewiring of biological networks. PLoS Comput Biol. 7:e1001050.
51. Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA. 1989. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75-77.
52. Spassov DS, Jurecic R. 2003. The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life. 55:359-366.
53. Sun J, Jiang H, Flores R, Wen J. 2010. Gene duplication in the genome of parasitic Giardia lamblia. BMC Evol Biol. 10:49.
54. Tam PP, Barrette-Ng IH, Simon DM, Tam MW, Ang AL, Muench DG. 2010. The Puf family of RNA-binding proteins in plants: phylogeny, structural modeling, activity and subcellular localization. BMC Plant Biol. 10:44.
55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
56. Tanay A, Regev A, Shamir R. 2005. Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci USA. 102:7203-7208. (Pubitemid 40696358)
57. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
58. Wickens M, Bernstein DS, Kimble J, Parker R. 2002. A PUF family portrait: 3'UTR regulation as a way of life. Trends Genet. 18:150-157. (Pubitemid 34164641)
59. Woodson JD, Chory J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet. 9:383-395. (Pubitemid 351559601)
60. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 8:206-216.
61. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA. 2003. The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol. 20:1377-1419. (Pubitemid 37086669)