The evolution of gene expression and the transcriptome-phenotype relationship

Seminars in Cell and Developmental Biology

Volumn 23, Issue 2, 2012, Pages 222-229

  Harrison, Peter W ^a   Wright, Alison E ^a   Mank, Judith E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Adaptive evolution; Complex phenotypes; Gene expression evolution; Gene regulation; Transcriptomics

Indexed keywords

TRANSCRIPTOME;

ENVIRONMENTAL FACTOR; EPIGENETICS; EVOLUTIONARY ADAPTATION; EVOLUTIONARY RATE; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; GENETIC CONSERVATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; MICROARRAY ANALYSIS; PHENOTYPE; QUANTITATIVE TRAIT LOCUS; REGULATORY MECHANISM; REVIEW; RNA SEQUENCE; SPECIES DIFFERENCE;

EID: 84858794348     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.12.004     Document Type: Review

References (91)

1. Hoekstra H.E., Coyne J.A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 2007, 61:995-1016.
2. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
3. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
4. Clark A.G., Eisen M.B., Smith D.R., Bergman C.M., Oliver B., Markow T.A., et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450:203-218.
5. Clark A.G., Glanowski S., Nielsen R., Thomas P.D., Kejariwal A., Todd M.A., et al. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 2003, 302:1960-1963.
6. Rubin C-J., Zody M.C., Eriksson J., Meadows J.R.S., Sherwood E., Webster M.T., et al. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 2010, 464:587-591.
7. Sabeti P.C., Schaffner S.F., Fry B., Lohmueller J., Varilly P., Shamovsky O., et al. Positive natural selection in the human lineage. Science 2006, 312:1614-1620.
8. Yi X., Liang Y., Huerta-Sanchez E., Jin X., Cuo Z.X.P., Pool J.E., et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 2010, 329:75-78.
9. Manceau M., Domingues V.S., Mallarino R., Hoekstra H.E. The developmental role of agouti in color pattern evolution. Science 2011, 331:1062-1065.
10. Rebeiz M., Pool J.E., Kassner V.A., Aquadro C.F., Carroll S.B. Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 2009, 326:1663-1667.
11. Abzhanov A., Kuo W.P., Hartmann C., Grant B.R., Grant P.R., Tabin C.J. The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 2006, 442:563-567.
12. Ometto L., Shoemaker D., Ross K.G., Keller L. Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species. Mol Biol Evol 2010, 28:1381-1392.
13. Wurm Y., Wang J., Keller L. Changes in reproductive roles are associated with changes in gene expression in fire ant queens. Mol Ecol 2010, 19:1200-1211.
14. Wyman M.J., Agrawal A.F., Rowe L. Condition-dependence of the sexually dimorphic transcriptome in Drosophila melanogaster. Evolution 2010, 64:1836-1848.
15. Ranz J.M., Castillo-Davis C.I., Meiklejohn C.D., Hartl D.L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 2003, 300:1742-1745.
16. Pancaldi V., Schubert F., Bähler J. Meta-analysis of genome regulation and expression variability across hundreds of environmental and genetic perturbations in fission yeast. Mol Biosyst 2010, 6:543-552.
17. Brawand D., Soumillon M., Necsulea A., Julien P., Csardi G., Harrigan P., et al. The evolution of gene expression levels in mammalian organs. Nature 2011, 478:343-348.
18. Grath S., Baines J., Parsch J. Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup. BMC Evol Biol 2009, 9:291.
19. Jiang Z-F., Machado C.A. Evolution of sex-dependent gene expression in three recently diverged species of Drosophila. Genetics 2009, 183:1175-1185.
20. Naurin S., Hansson B., Hasselquist D., Kim Y-H., Bensch S. The sex-biased brain: sexual dimorphism in gene expression in two species of songbirds. BMC Genomics 2011, 12:37.
21. Zhang Y., Sturgill D., Parisi M., Kumar S., Oliver B. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 2007, 450:233-238.
22. Kimura M. The neutral theory of molecular evolution 1983, Cambridge University Press, Cambridge.
23. Hartl D.L., Clark A.G. Principles of population genetics 1997, Sinauer Associates Inc., MA, SunderlandMA. 3rd ed.
24. Oleksiak M.F., Churchill G.A., Crawford D.L. Variation in gene expression within and among natural populations. Nat Genet 2002, 32:261-266.
25. Rifkin S.A., Kim J., White K.P. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 2003, 33:138-144.
26. Lemos B., Meiklejohn C.D., Cáceres M., Hartl D.L. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 2005, 59:126-137.
27. Jermann T.M., Opitz J.G., Stackhouse J., Benner S.A. Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 1995, 374:57-59.
28. Khaitovich P., Weiss G., Lachmann M., Hellmann I., Enard W., Muetzel B., et al. A neutral model of transcriptome evolution. PLoS Biol 2004, 2:e132.
29. Gilad Y., Oshlack A., Smyth G.K., Speed T.P., White K.P. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 2006, 440:242-245.
30. Jordan I.K., Mariño-Ramírez L., Koonin E.V. Evolutionary significance of gene expression divergence. Gene 2005, 345:119-126.
31. Khaitovich P., Hellmann I., Enard W., Nowick K., Leinweber M., Franz H., et al. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 2005, 309:1850-1854.
32. Mank J.E., Hultin-Rosenberg L., Zwahlen M., Ellegren H. Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. Am Nat 2008, 171:35-43.
33. Khaitovich P., Pääbo S., Weiss G. Toward a neutral evolutionary model of gene expression. Genetics 2005, 170:929-939.
34. Chaix R., Somel M., Kreil D.P., Khaitovich P., Lunter G.A. Evolution of primate gene expression: drift and corrective sweeps. Genetics 2008, 180:1379-1389.
35. Gilad Y., Rifkin S.A., Pritchard J.K. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet 2008, 24:408-415.
36. Khaitovich P. Brain expression - is it all in our SNPs?. Mol Syst Biol 2007, 3:155.
37. Majewski J., Pastinen T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet 2011, 27:72-79.
38. Gilad Y., Oshlack A., Rifkin S.A. Natural selection on gene expression. Trends Genet 2006, 22:456-461.
39. Jones P.A., Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001, 293:1068-1070.
40. Valencia-Sanchez M.A., Liu J.D., Hannon G.J., Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006, 20:515-524.
41. Blekhman R., Marioni J.C., Zumbo P., Stephens M., Sex-specific Gilad Y. lineage-specific alternative splicing in primates. Genome Res 2010, 20:180-189.
42. Prince E.G., Kirkland D., Demuth J.P. Hyperexpression of the X chromosome in both sexes results in extensive female-bias of X-linked gene in the flour beetle. Genome Biol Evol 2010, 2:336-346.
43. Telonis-Scott M., Kopp A., Wayne M.L., Nuzhdin S.V., McIntyre L.M. Sex-specific splicing in Drosophila: widespread occurrence, tissue specificity and evolutionary conservation. Genetics 2009, 181:421-434.
44. Licatalosi D.D., Darnell R.B. RNA processing and its regulation: global insights into biological networks. Nat Rev Genet 2010, 11:75-87.
45. Hyman E., Kauraniemi P., Hautaniemi S., Wolf M., Mousses S., Rozenblum E., et al. Impact of DNA amplification on gene expression patterns in breast cancer. Cancer Res 2002, 62:6240-6245.
46. Mank J.E. The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet 2009, 25:226-233.
47. Pollack J.R., Sørlie T., Perou C.M., Rees C.A., Jeffrey S.S., Lonning P.E., et al. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci USA 2002, 99:12963-12968.
48. Fu N., Drinnenberg I., Kelso J., Wu J-R., Paeaebo S., Zeng R., et al. Comparison of protein and mRNA expression evolution in humans and chimpanzees. PloS One 2007, 2:e216.
49. Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., et al. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
50. Idaghdour Y., Storey J.D., Jadallah S.J., Gibson G. A genome-wide gene expression signature of environmental geography in leukocytes of Moroccan amazighs. PLoS Genet 2008, 4:e1000052.
51. Whitehead A., Crawford D.L. Neutral and adaptive variation in gene expression. Proc Natl Acad Sci USA 2006, 103:5425-5430.
52. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
53. Hager R., Cheverud J.M., Leamy L.J., Wolf J.B. Sex dependent imprinting effects on complex traits in mice. BMC Evol Biol 2008, 8:303.
54. Obermann C., Meyer E., Prager S., Tomiuk J., Wollmann H.A., Eggermann T. Searching for genomic variants in IGF2 and CDKN1C in Silver-Russell syndrome patients. Mol Genet Metab 2004, 82:246-250.
55. Day T., Bonduriansky R. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 2004, 167:1537-1546.
56. Van Cleve J., Feldman M.W. Sex-specific viability, sex linkage and dominance in genomic imprinting. Genetics 2007, 176:1101-1118.
57. Ellegren H., Parsch J. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 2007, 8:689-698.
58. Good J.M., Nachman M.W. Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol Biol Evol 2005, 22:1044-1052.
59. Hovatta I., Zapala M.A., Broide R.S., Schadt E.E., Libiger O., Schork N.J., et al. DNA variation and brain region-specific expression profiles exhibit different relationships between inbred mouse strains: implications for eQTL mapping studies. Genome Biol 2007, 8:R25.
60. Lemos B., Bettencourt B.R., Meiklejohn C.D., Hartl D.L. Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Mol Biol Evol 2005, 22:1345-1354.
61. Meiklejohn C.D., Parsch J., Ranz J.M., Hartl D.L. Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci USA 2003, 100:9894-9899.
62. Nuzhdin S.V., Wayne M.L., Harmon K.L., McIntyre L.M. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol 2004, 21:1308-1317.
63. Shapiro M.D., Marks M.E., Peichel C.L., Blackman B.K., Nereng K.S., Jonsson B., et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 2004, 428:717-723.
64. Nagalakshmi U., Wang Z., Waern K., Shou C., Raha D., Gerstein M., et al. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320:1344-1349.
65. Morin R., Bainbridge M., Fejes A., Hirst M., Krzywinski M., Pugh T., et al. Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. Biotechniques 2008, 45:81-94.
66. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
67. Robertson G., Schein J., Chiu R., Corbett R., Field M., Jackman S.D., et al. De novo assembly and analysis of RNA-seq data. Nat Methods 2010, 7:909-912.
68. Feldmeyer B., Wheat C.W., Krezdorn N., Rotter B., Pfenninger M. Short read Illumina data for the de novo assembly of a non-model snail species transcriptome (Radix balthica, Basommatophora, Pulmonata), and a comparison of assembler performance. BMC Genomics 2011, 12:317.
69. Santure A.W., Gratten J., Mossman J.A., Sheldon B.C., Slate J. Characterisation of the transcriptome of a wild great tit Parus major population by next generation sequencing. BMC Genomics 2011, 12:283.
70. Gilad Y., Rifkin S.A., Bertone P., Gerstein M., White K.P. Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. Genome Res 2005, 15:674-680.
71. Chang P.L., Dunham J.P., Nuzhdin S.V., Arbeitman M.N. Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics 2011, 12:364.
72. Chen C., Ai H., Ren J., Li W., Li P., Qiao R., et al. A global view of porcine transcriptome in three tissues from a full-sib pair with extreme phenotypes in growth and fat deposition by paired-end RNA sequencing. BMC Genomics 2011, 12:448.
73. Wilhelm B.T., Marguerat S., Watt S., Schubert F., Wood V., Goodhead I., et al. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 2008, 453:1239-1243.
74. Pal S, Gupta R, Kim H, Wickramasinghe P, Baubet V, Showe LC, et al. Alternative transcription exceeds alternative splicing in generating the transcriptome diversity of cerebellar development. Genome Res, . doi:10.1101/gr.120535.111.
75. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10:57-63.
76. Churchill G.A. Fundamentals of experimental design for cDNA microarrays. Nat Genet 2002, 32:490-495.
77. Bainbridge M.N., Warren R.L., Hirst M., Romanuik T., Zeng T., Go A., et al. Analysis of the prostate cancer cell line LNCaP transcriptome using a sequencing-by-synthesis approach. BMC Genomics 2006, 7:246.
78. Hashimoto S-i Qu W., Ahsan B., Ogoshi K., Sasaki A., Nakatani Y., et al. High-resolution analysis of the 5'-end transcriptome using a next generation DNA sequencer. PLoS One 2009, 4:e4108.
79. Marioni J.C., Mason C.E., Mane S.M., Stephens M., Gilad Y.R.N.A-seq. An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 2008, 18:1509-1517.
80. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
81. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106.
82. Auer P.L., Doerge R.W. Statistical design and analysis of RNA sequencing data. Genetics 2010, 185:405-416.
83. Arbeitman M.N., Furlong E.E.M., Imam F., Johnson E., Null B.H., Baker B.S., et al. Gene expression during the life cycle of Drosophila melanogaster. Science 2002, 297:2270-2275.
84. Mank J.E., Nam K., Brunström B., Ellegren H. Ontogenetic complexity of sexual dimorphism and sex-specific selection. Mol Biol Evol 2010, 27:1570-1578.
85. Domazet-Loso T., Tautz D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 2010, 468:815-818.
86. Kalinka A.T., Varga K.M., Gerrard D.T., Preibisch S., Corcoran D.L., Jarrells J., et al. Gene expression divergence recapitulates the developmental hourglass model. Nature 2010, 468:811-814.
87. López-Maury L., Marguerat S., Bähler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 2008, 9:583-593.
88. Hansen K.D., Brenner S.E., Dudoit S. Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 2010, 38:e131.
89. Zheng W., Chung L.M., Zhao H. Bias detection and correction in RNA-sequencing data. BMC Bioinformatics 2011, 12:290.
90. Hafner M., Landgraf P., Ludwig J., Rice A., Ojo T., Lin C., et al. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 2008, 44:3-12.
91. Robertson G., Hirst M., Bainbridge M., Bilenky M., Zhao Y., Zeng T., et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 2007, 4:651-657.