Genetic Influences on Translation in Yeast

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Albert, Frank W ^a   Muzzey, Dale ^b   Weissman, Jonathan S ^b   Kruglyak, Leonid ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; MESSENGER RNA; TRANS ACTING FACTOR;

ALLELE; ARTICLE; DIPLOIDY; FUNGAL GENE; FUNGAL STRAIN; GENE EXPRESSION; GENETIC DIFFERENCE; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN FOOTPRINTING; RNA ANALYSIS; RNA HYBRIDIZATION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENCE; STRAIN DIFFERENCE; YEAST; BIOSYNTHESIS; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; HUMAN; METABOLISM; PROTEIN SYNTHESIS; RIBOSOME; SEQUENCE ALIGNMENT;

ALLELES; DATABASES, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HUMANS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

EID: 84908326045     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004692     Document Type: Article

References (62)

1. Brem RB, Yvert G, Clinton R, Kruglyak L, (2002) Genetic Dissection of Transcriptional Regulation in Budding Yeast. Science (New York, NY) 296: 752–755.
2. Rockman MV, Kruglyak L, (2006) Genetics of global gene expression. Nature Reviews Genetics 7: 862–872.
3. Lappalainen T, Sammeth M, Friedländer MR, Hoen PAC', Monlong J, et al. (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501: 506–511.
4. Foss EJ, Foss EJ, Radulovic D, Radulovic D, Shaffer SA, et al. (2007) Genetic basis of proteome variation in yeast. Nature Genetics 39: 1369–1375.
5. Foss EJ, Radulovic D, Shaffer SA, Goodlett DR, Kruglyak L, et al. (2011) Genetic Variation Shapes Protein Networks Mainly through Non-transcriptional Mechanisms. PLoS Biology 9: e1001144 doi:10.1371/journal.pbio.1001144.s010
6. Ghazalpour A, Bennett B, Petyuk VA, Orozco L, Hagopian R, et al. (2011) Comparative Analysis of Proteome and Transcriptome Variation in Mouse. PLoS Genetics 7: e1001393 doi:10.1371/journal.pgen.1001393.s015
7. Damerval C, Maurice A, Josse JM, de Vienne D, (1994) Quantitative trait loci underlying gene product variation: a novel perspective for analyzing regulation of genome expression. Genetics 137: 289–301.
8. Albert FW, Treusch S, Shockley AH, Bloom JS, Kruglyak L, (2014) Genetics of single-cell protein abundance variation in large yeast populations. Nature 506: 494–497.
9. Skelly DA, Skelly DA, Merrihew GE, Merrihew GE, Riffle M, et al. (2013) Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast. Genome Research 23: 1496–1504.
10. Wu L, Candille SI, Choi Y, Xie D, Jiang L, et al. (2013) Variation and genetic control of protein abundance in humans. Nature 499: 79–82.
11. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337–342.
12. Li JJ, Bickel PJ, Biggin MD, (2014) System wide analyses have underestimated protein abundances and the importance of transcription in mammals. PeerJ 2: e270 doi:10.7717/peerj.270
13. Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS, (2009) Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling. Science (New York, NY) 324: 218–223.
14. Wittkopp PJ, Haerum BK, Clark AG, (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88.
15. Wittkopp PJ, Haerum BK, Clark AG, (2008) Regulatory changes underlying expression differences within and between Drosophila species. Nature Genetics 40: 346–350.
16. Bloom JS, Khan Z, Kruglyak L, Singh M, Caudy AA, (2009) Measuring differential gene expression by short read sequencing: quantitative comparison to 2-channel gene expression microarrays. BMC Genomics 10: 221.
17. Emerson JJ, Hsieh L-C, Sung H-M, Wang T-Y, Huang C-J, et al. (2010) Natural selection on cis and trans regulation in yeasts. Genome Research 20: 826–836.
18. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, et al. (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464: 768–772.
19. Montgomery SB, Sammeth M, Gutierrez-Arcelus M, Lach RP, Ingle C, et al. (2010) Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773–777.
20. Sonenberg N, Hinnebusch AG, (2009) Regulation of Translation Initiation in Eukaryotes: Mechanisms and Biological Targets. Cell 136: 731–745.
21. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, et al. (2011) Ribosome-Mediated Specificity in Hox mRNA Translation and Vertebrate Tissue Patterning. Cell 145: 383–397.
22. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS, (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 7: 1534–1550.
23. Preiss T, Baron-Benhamou J, Ansorge W, Hentze MW, (2003) Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Biol 10: 1039–1047.
24. Lackner DH, Schmidt MW, Wu S, Wolf DA, Bähler J, (2012) Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast. Genome Biol 13: R25.
25. Halbeisen RE, Gerber AP, (2009) Stress-Dependent Coordination of Transcriptome and Translatome in Yeast. PLoS Biology 7: e1000105 doi:10.1371/journal.pbio.1000105
26. MacKay VL, Li X, Flory MR, Turcott E, Law GL, et al. (2004) Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteomics 3: 478–489.
27. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, et al. (2007) A Network of Multiple Regulatory Layers Shapes Gene Expression in Fission Yeast. Molecular Cell 26: 145–155.
28. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences 100: 9440–9445.
29. Smith EN, Kruglyak L, (2008) Gene–Environment Interaction in Yeast Gene Expression. PLoS Biology 6: e83 doi:10.1371/journal.pbio.0060083.st004
30. Soneson C, Delorenzi M, (2013) A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics 14: 91.
31. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
32. Ronald J, Brem RB, Whittle J, Kruglyak L, (2005) Local Regulatory Variation in Saccharomyces cerevisiae. PLoS Genetics 1: e25 doi:10.1371/journal.pgen.0010025
33. Warton DI, Wright IJ, Falster DS, Westoby M, (2006) Bivariate line-fitting methods for allometry. Biological Reviews 81: 259.
34. McManus CJ, May GE, Spealman P, Shteyman A, (2014) Ribosome profiling reveals post-transcriptional buffering of divergent gene expression in yeast. Genome Research 24: 422–430.
35. Artieri CG, Fraser HB, (2014) Evolution at two levels of gene expression in yeast. Genome Research 24: 411–421.
36. MacArthur DG, Balasubramanian S, Frankish A, Huang N, Morris J, et al. (2012) A Systematic Survey of Loss-of-Function Variants in Human Protein-Coding Genes. Science (New York, NY) 335: 823–828.
37. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES, (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241–254.
38. Godard P, Urrestarazu A, Vissers S, Kontos K, Bontempi G, et al. (2007) Effect of 21 Different Nitrogen Sources on Global Gene Expression in the Yeast Saccharomyces cerevisiae. Molecular and Cellular Biology 27: 3065–3086.
39. Williams I, Richardson J, Starkey A, Stansfield I, (2004) Genome-wide prediction of stop codon readthrough during translation in the yeast Saccharomyces cerevisiae. Nucleic Acids Research 32: 6605–6616.
40. Parts L, Liu YC, Tekkedil M, Steinmetz LM, Caudy AA, et al. (2014) Heritability and genetic basis of protein level variation in an outbred population. Genome Research 24 doi:10.1101/gr.170506.113
41. Wallace EWJ, Airoldi EM, Drummond DA, (2013) Estimating Selection on Synonymous Codon Usage from Noisy Experimental Data. Mol Biol Evol 30: 1438–1453.
42. Muzzey D, Sherlock G, Weissman JS, (2014) Extensive and coordinated control of allele-specific expression by both transcription and translation in Candida albicans. Genome Research 24: 963–973.
43. Dahan O, Gingold H, Pilpel Y, (2011) Regulatory mechanisms and networks couple the different phases of gene expression. Trends in Genetics 27: 316–322.
44. Zid BM, O'Shea EK, (2014) Promoter sequences direct cytoplasmic localization and translation of mRNAs during starvation in yeast. Nature doi:10.1038/nature13578
45. Harel-Sharvit L, Eldad N, Haimovich G, Barkai O, Duek L, et al. (2010) RNA Polymerase II Subunits Link Transcription and mRNA Decay to Translation. Cell 143: 552–563.
46. Parker R, (2012) RNA degradation in Saccharomyces cerevisae. Genetics 191: 671–702.
47. Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB, (2013) Rate-limiting steps in yeast protein translation. Cell 153: 1589–1601.
48. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, et al. (2003) The UCSC Genome Browser Database. Nucleic Acids Research 31: 51–54.
49. Dermitzakis ET, (2012) Cellular genomics for complex traits. Nature Reviews Genetics doi:10.1038/nrg3115
50. Gaffney DJ, (2013) Global Properties and Functional Complexity of Human Gene Regulatory Variation. PLoS Genetics 9: e1003501 doi:10.1371/journal.pgen.1003501
51. Bloom JS, Ehrenreich IM, Loo WT, Lite T-LV, Kruglyak L, (2013) Finding the sources of missing heritability in a yeast cross. Nature 494: 234–237.
52. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, et al. (2012) High-Resolution View of the Yeast Meiotic Program Revealed by Ribosome Profiling. Science (New York, NY) 335: 552–557.
53. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.
54. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
55. Skelly DA, Johansson M, Madeoy J, Wakefield J, Akey JM, (2011) A powerful and flexible statistical framework for testing hypotheses of allele-specific gene expression from RNA-seq data. Genome Research 21: 1728–1737.
56. Bergstrom A, Simpson JT, Salinas F, Barre B, Parts L, et al. (2014) A high-definition view of functional genetic variation from natural yeast genomes. Mol Biol Evol
57. Warton DI, Duursma RA, Falster DS, Taskinen S, (2011) smatr 3- an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257–259.
58. Coolon JD, McManus CJ, Stevenson KR, Graveley BR, Wittkopp PJ, (2014) Tempo and mode of regulatory evolution in Drosophila. Genome Research 24 doi:10.1101/gr.163014.113
59. Dabney A, Storey JD, (2004) Q-value estimation for false discovery rate control. Medicine 344: 539–548.
60. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 289–300.
61. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, et al. (2010) Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26: 2069–2070.
62. Hahne F, Durinck S, Ivanek R, Mueller A, Lianoglou S, et al. (n.d.) Gviz: Plotting data and annotation information along genomic coordinates. R package version 1.7.4.