Virtual genomes in flux: An interplay of neutrality and adaptability explains genome expansion and streamlining

Genome Biology and Evolution

Volumn 4, Issue 3, 2012, Pages 212-229

  Cuypers, Thomas D ^a   Hogeweg, Paulien ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Evolution of complexity; Evolutionary modeling; Gene content; Genome expansion; Streamlining; Virtual cell

Indexed keywords

ANIMAL; ARTICLE; GENETICS; GENOME; GENOME SIZE; HUMAN; MOLECULAR EVOLUTION; PHYLOGENY;

ANIMALS; EVOLUTION, MOLECULAR; GENOME; GENOME SIZE; HUMANS; PHYLOGENY;

EID: 84863208931     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evr141     Document Type: Article

References (72)

1. Aldana M, Balleza E, Kauffman S, Resendiz O. 2007. Robustness and evolvability in genetic regulatory networks. J Theor Biol. 245:433-448.
2. Ames RM, et al. 2010. Gene duplication and environmental adaptation within yeast populations. Genome Biol Evol. 2:591-601.
3. Andersson DI, Hughes D. 2009. Gene amplification and adaptive evolution in bacteria. Annu Rev Genet. 43(1):167-195.
4. Archibald JD. 1999. Divergence times of eutherian mammals. Science 285(5436):2031.
5. Battistuzzi F, Feijao A, Hedges SB. 2004. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol. 4(1):44.
6. Blanc G, Wolfe KH. 2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16(7):1667-1678.
7. Chen P, Shakhnovich EI. 2009. Lethal mutagenesis in viruses and bacteria. Genetics 183(2):639-650.
8. Chen P, Shakhnovich EI. 2010. Thermal adaptation of viruses and bacteria. Biophys J. 98(7):1109-1118.
9. Chernikova D, Motamedi S, Csuros M, Koonin E, Rogozin I. 2011. A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes. Biol Direct. 6(1):26.
10. Ciliberti S, Martin OC, Wagner A. 2007a. Innovation and robustness in complex regulatory gene networks. Proc Natl Acad Sci U S A. 104: 13591-13596.
11. Ciliberti S, Martin OC, Wagner A. 2007b. Robustness can evolve gradually in complex regulatory gene networks with varying topology. PLoS Comput Biol. 3:e15.
12. Cordero OX, Hogeweg P. 2007. Large changes in regulome size herald the main prokaryotic lineages. Trends Genet. 23:488-493.
13. Crombach A, Hogeweg P. 2007. Chromosome rearrangements and the evolution of genome structuring and adaptability. Mol Biol Evol. 24(5):1130-1139.
14. Crombach A, Hogeweg P. 2008. Evolution of evolvability in gene regulatory networks. PLoS Comput Biol. 4(7):e1000112.
15. Csu″rös M, Miklós I. 2009. Streamlining and large ancestral genomes in archaea inferred with a phylogenetic birth-and-death model. Mol Biol Evol. 26(9):2087-2095.
16. David LA, Alm EJ. 2010. Rapid evolutionary innovation during an archaean genetic expansion. Nature. 469:93-96.
17. De Bodt S, Maere S, Van de Peer Y. 2005. Genome duplication and the origin of angiosperms. Trends Ecol Evol. 20(11):591-597.
18. de Boer FK, Hogeweg P. 2010. Eco-evolutionary dynamics, coding structure and the information threshold. BMC Evol Biol. 10:361.
19. Demuth JP, Hahn MW. 2009. The life and death of gene families. Bioessays 31(1):29-39.
20. Doolittle WF, et al. 2003. How big is the iceberg of which organellar genes in nuclear genomes are but the tip? Philos Trans R Soc Lond B Biol Sci. 358(1429):39-58.
21. Dujon B, et al. 2004. Genome evolution in yeasts. Nature 430(6995):35-44.
22. Dunham MJ, et al. 2002. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 99(25):16144-16149.
23. Fawcett JA, Maere S, Van de Peer Y. 2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci U S A. 106(14):5737-5742.
24. Ferea TL, Botstein D, Brown PO, Rosenzweig RF. 1999. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci U S A. 96(17):9721-9726.
25. Francino MP. 2005. An adaptive radiation model for the origin of new gene functions. Nat Genet. 37(6):573-578.
26. Gregory TR. 2005. The evolution of the genome. 1st ed. San Diego (CA): Academic Press.
27. Hall DW, Joseph SB. 2010. A high frequency of beneficial mutations across multiple fitness components in Saccharomyces cerevisiae. Genetics 185:1397-1409.
28. Harcet M, et al. 2010. Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans. Mol Biol Evol. 27:2747-2756.
29. Huynen MA, Stadler PF, Fontana W. 1996. Smoothness within ruggedness: the role of neutrality in adaptation. Proc Natl Acad Sci U S A. 93(1):397-401.
30. Ihmels J, et al. 2005. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309(5736):938-940.
31. Jordan IK, Makarova KS, Spouge JL, Wolf YI, Koonin EV. 2001. Lineage- Specific gene expansions in bacterial and archaeal genomes. Genome Res. 11(4):555-565.
32. Khachane AN, Timmis KN, Martins dos Santos VAP. 2007. Dynamics of reductive genome evolution in mitochondria and obligate intracellular microbes. Mol Biol Evol. 24(2):449-456.
33. Knibbe C, Coulon A, Mazet O, Fayard J, Beslon G. 2007. A long-term evolutionary pressure on the amount of noncoding DNA. Mol Biol Evol. 24(10):2344-2353.
34. Knibbe C, Mazet O, Chaudier F, Fayard JM, Beslon G. 2007. Evolutionary coupling between the deleteriousness of gene mutations and the amount of non-coding sequences. J Theor Biol. 244:621-630.
35. Koonin EV. 2007. The biological big bang model for the major transitions in evolution. Biol Direct. 2:21.
36. Koonin EV. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11(5):209.
37. Kuo C, Ochman H. 2009. Deletional bias across the three domains of life. Genome Biol Evol. 1:145-152.
38. Kurland CG, Andersson SGE. 2000. Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev. 64(4):786-820.
39. Lavoie H, et al. 2010. Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol. 8(3): e1000329.
40. Lespinet O, Wolf YI, Koonin EV, Aravind L. 2002. The role of lineagespecific gene family expansion in the evolution of eukaryotes. Genome Res. 12(7):1048-1059.
41. Lynch M. 2006a. The origins of eukaryotic gene structure. Mol Biol Evol. 23(2):450-468.
42. Lynch M. 2006b. Streamlining and simplification of microbial genome architecture. Annu Rev Microbiol. 60(1):327-349.
43. Lynch M. 2007. The evolution of genetic networks by non-adaptive processes. Nat Rev Genet. 8:803-813.
44. Lynch M, Conery JS. 2003a. The evolutionary demography of duplicate genes. J Struct Funct Genomics. 3(1):35-44.
45. Lynch M, Conery JS. 2003b. The origins of genome complexity. Science 302:1401-1404.
46. Makarova K, et al. 2006. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A. 103(42):15611-15616.
47. Makarova KS, Wolf YI, Mekhedov SL, Mirkin BG, Koonin EV. 2005. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 33(14): 4626-4638.
48. Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M. 2007. Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol. 17(12):1007-1013.
49. Neyfakh AA, Baranova NN, Mizrokhi LJ. 2006. A system for studying evolution of life-like virtual organisms. Biol Direct. 1:21.
50. Ouzounis CA, Kunin V, Darzentas N, Goldovsky L. 2005. A minimal estimate for the gene content of the last universal common ancestor-exobiology from a terrestrial perspective. Res Microbiol. 157(1):57-68.
51. Parter M, Kashtan N, Alon U. 2008. Facilitated variation: how evolution learns from past environments to generalize to new environments. PLoS Comput Biol. 4(11):e1000206.
52. Putnam NH, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317(5834):86-94.
53. Redon R, et al. 2006. Global variation in copy number in the human genome. Nature 444(7118):444-454.
54. Sakharkar KR, Dhar PK, Chow VTK. 2004. Genome reduction in prokaryotic obligatory intracellular parasites of humans: a comparative analysis. Int J Syst Evol Microbiol. 54(6): 1937-1941.
55. Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH. 2006. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440(7082):341-345.
56. Sheridan P, Freeman K, Brenchley J. 2003. Estimated minimal divergence times of the major bacterial and archaeal phyla. Geomicrobiol J. 20(1):1-14.
57. Sicheritz-Pontén T, Kurland CG, Andersson SGE. 1998. A phylogenetic analysis of the cytochrome b and cytochrome c oxidase i genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim Biophys Acta. 1365(3):545-551.
58. Sliwa P. 2005. Loss of dispensable genes is not adaptive in yeast. Proc Natl Acad Sci U S A. 102:17670-17674.
59. Snel B, Bork P, Huynen MA. 2002. Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res. 12:17-25.
60. Soyer OS, Bonhoeffer S. 2006. Evolution of complexity in signaling pathways. Proc Natl Acad Sci U S A. 103:16337-16342.
61. Srivastava M, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720-726.
62. Teichmann SA, Babu MM. 2004. Gene regulatory network growth by duplication. Nat Genet. 36:492-496.
63. ten Tusscher K, Hogeweg P. 2009. The role of genome and gene regulatory network canalization in the evolution of multi-trait polymorphisms and sympatric speciation. BMC Evol Biol. 9(1):159.
64. Tsong AE, Tuch BB, Li H, Johnson AD. 2006. Evolution of alternative transcriptional circuits with identical logic. Nature 443(7110):415-420.
65. Tuller T, Birin H, Gophna U, Kupiec M, Ruppin E. 2010. Reconstructing ancestral gene content by coevolution. Genome Res. 20(1):122-132.
66. Van de Peer Y, Maere S, Meyer A. 2009. The evolutionary significance of ancient genome duplications. Nat Rev Genet. 10(10):725-732.
67. van Ham RCHJ, et al. 2003. Reductive genome evolution in buchnera aphidicola. Proc Natl Acad Sci U S A. 100(2):581-586.
68. van Hoek MJA, Hogeweg P. 2009. Metabolic adaptation after whole genome duplication. Mol Biol Evol. 26(11):2441-2453.
69. van Nimwegen E, Crutchfield JP, Huynen M. 1999. Neutral evolution of mutational robustness. Proc Natl Acad Sci U S A. 96(17): 9716-9720.
70. Wloch DM, Szafraniec K, Borts RH, Korona R. 2001. Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159(2):441-452.
71. Zeldovich KB, Chen P, Shakhnovich BE, Shakhnovich EI. 2007. A firstprinciples model of early evolution: emergence of gene families, species, and preferred protein folds. PLoS Comput Biol. 3(7): e139.
72. Zmasek CM, Godzik A. 2011. Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biol. 12(1):R4.