A Synergism between Adaptive Effects and Evolvability Drives Whole Genome Duplication to Fixation

PLoS Computational Biology

Volumn 10, Issue 4, 2014, Pages

  Cuypers, Thomas D ^a   Hogeweg, Paulien ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GENES;

ENVIRONMENTAL CHANGE; ENVIRONMENTAL SPECIES; EUKARYOTICS; EVOLUTIONARY HISTORY; EVOLVABILITY; GENOME DUPLICATION; INTERACTING GENES; REGULATORY NETWORK; SUBFUNCTIONALIZATION; VIRTUAL CELLS;

MACHINERY;

ARTICLE; CELL LINEAGE; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; EUKARYOTE; EVOLUTIONARY ADAPTATION; GENE CONTROL; GENE DELETION; GENE DUPLICATION; GENE INTERACTION; GENE MUTATION; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC VARIABILITY; MUTATION RATE; POINT MUTATION; SIMULATION; ADAPTATION; GENETICS; GENOME; MOLECULAR EVOLUTION;

ADAPTATION, PHYSIOLOGICAL; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME;

EID: 84901325461     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003547     Document Type: Article

References (61)

1. Gregory TR, (2001) Coincidence, coevolution, or causation? DNA content, cell size, and the c-value enigma. Biological reviews of the Cambridge Philosophical Society 76: 65-101.
2. 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. Research in Microbiology 157: 57-68.
3. Koonin EV, (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biology 11: 209.
4. Zmasek CM, Godzik A, (2011) Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biology 12: R4.
5. Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, et al. (2012) A genome triplication associated with early diversification of the core eudicots. Genome Biology 13: R3.
6. Stelzer CP, Riss S, Stadler P, (2011) Genome size evolution at the speciation level: The cryptic species complex brachionus plicatilis (rotifera). BMC Evolutionary Biology 11: 90.
7. Ohno S (1970) Evolution by gene duplication. Springer-Verlag.
8. Dehal P, Boore JL, (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology 3: e314.
9. Nakatani Y, Takeda H, Kohara Y, Morishita S, (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Research 17: 1254-1265.
10. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
11. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, et al. (2004) Genome duplication in the teleost fish tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957.
12. 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: 341-345.
13. Amborella Genome Project (2013) The amborella genome and the evolution of flowering plants. Science 342: 1241089.
14. Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, et al. (2011) Recently formed polyploid plants diversify at lower rates. Science 333: 1257.
15. Brochmann C, Brysting AK, Alsos IG, Borgen L, Grundt HH, et al. (2004) Polyploidy in arctic plants. Biological Journal of the Linnean Society 82: 521536.
16. Barrier M, Baldwin BG, Robichaux RH, Purugganan MD, (1999) Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the hawaiian silversword alliance (asteraceae) inferred from floral homeotic gene duplications. Molecular Biology and Evolution 16: 1105-1113.
17. Beest Mt, Roux JJL, Richardson DM, Brysting AK, Suda J, et al. (2012) The more the better? the role of polyploidy in facilitating plant invasions. Annals of Botany 109: 19-45.
18. Conant GC, Wolfe KH, (2007) Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Molecular Systems Biology 3: 129.
19. van Hoek MJA, Hogeweg P, (2009) Metabolic adaptation after whole genome duplication. Molecular Biology and Evolution 26: 2441-2453.
20. Fawcett JA, Maere S, Van de Peer Y, (2009) Plants with double genomes might have had a better chance to survive the CretaceousTertiary extinction event. Proceedings of the National Academy of Sciences of the United States of America 106: 5737-5742.
21. Van de Peer Y, Maere S, Meyer A, (2009) The evolutionary significance of ancient genome duplications. Nature Reviews Genetics 10: 725-732.
22. Kellis M, Birren BW, Lander ES, (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast saccharomyces cerevisiae. Nature 428: 617-624.
23. Aury JM, Jaillon O, Duret L, Noel B, Jubin C, et al. (2006) Global trends of whole-genome duplications revealed by the ciliate paramecium tetraurelia. Nature 444: 171-178.
24. Huminiecki L, Conant GC, (2012) Polyploidy and the evolution of complex traits. International Journal of Evolutionary Biology 2012: 292068.
25. Schnable JC, Wang X, Pires JC, Freeling M, (2012) Escape from preferential retention following repeated whole genome duplications in plants. Frontiers in plant science 3.
26. Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, et al. (2012) Contrasting patterns of evolution following whole genome versus tandem duplication events in populus. Genome Research 22: 95-105.
27. Bekaert M, Edger PP, Pires JC, Conant GC, (2011) Two-phase resolution of polyploidy in the arabidopsis metabolic network gives rise to relative and absolute dosage constraints. The Plant Cell Online 23: 1719-1728.
28. Freeling M, (2009) Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annual Review of Plant Biology 60: 433-453.
29. Force A, Lynch M, Pickett FB, Amores A, Yan YL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
30. Blanc G, Wolfe KH, (2004) Functional divergence of duplicated genes formed by polyploidy during arabidopsis evolution. The Plant Cell 16: 1679-1691.
31. Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, et al. (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of arabidopsis. Molecular Biology and Evolution 23: 469-478.
32. Papp B, Pl C, Hurst LD, (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
33. Blomme T, Vandepoele K, De Bodt S, Simillion C, Maere S, et al. (2006) The gain and loss of genes during 600 million years of vertebrate evolution. Genome biology 7: R43.
34. Hakes L, Pinney JW, Lovell SC, Oliver SG, Robertson DL, (2007) All duplicates are not equal: the difference between small-scale and genome duplication. Genome Biology 8: R209.
35. Wang Y, Wang X, Tang H, Tan X, Ficklin SP, et al. (2011) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS ONE 6 (12):: e28150.
36. Carretero-Paulet L, Fares MA, (2012) Evolutionary dynamics and functional specialization of plant paralogs formed by whole and small-scale genome duplications. Molecular Biology and Evolution 29: 3541-3551.
37. Birchler JA, Veitia RA, (2007) The gene balance hypothesis: From classical genetics to modern genomics. Plant Cell 19: 395-402.
38. Cuypers TD, Hogeweg P, (2012) Virtual genomes in flux: An interplay of neutrality and adaptability explains genome expansion and streamlining. Genome Biology and Evolution 4: 212-229.
39. 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 Research 33: 4626-4638.
40. De Bodt S, Maere S, Van de Peer Y, (2005) Genome duplication and the origin of angiosperms. Trends in Ecology & Evolution 20: 591-597.
41. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, et al. (2009) Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.
42. Gillis W, St John J, Bowerman B, Schneider S, (2009) Whole genome duplications and expansion of the vertebrate GATA transcription factor gene family. BMC Evolutionary Biology 9: 207.
43. Huminiecki L, Heldin CH, (2010) 2R and remodeling of vertebrate signal transduction engine. BMC Biology 8: 146.
44. Otto SP, (2007) The evolutionary consequences of polyploidy. Cell 131: 452-462.
45. Yona AH, Manor YS, Herbst RH, Romano GH, Mitchell A, et al. (2012) Chromosomal duplication is a transient evolutionary solution to stress. Proceedings of the National Academy of Sciences of the United States of America 109: 21010-21015.
46. Lynch M, (2006) The origins of eukaryotic gene structure. Molecular Biology and Evolution 23: 450-468.
47. Gray MW, Luke J, Archibald JM, Keeling PJ, Doolittle WF, (2010) Irremediable complexity? Science 330: 920-921.
48. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, et al. (2005) Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences of the United States of America 102: 5454-5459.
49. Hoof Av, (2005) Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 171: 1455-1461.
50. Wapinski I, Pfiffner J, French C, Socha A, Thompson DA, et al. (2010) Gene duplication and the evolution of ribosomal protein gene regulation in yeast. Proceedings of the National Academy of Sciences of the United States of America 107: 5505-5510.
51. Lynch M, Conery JS, (2003) The origins of genome complexity. Science 302: 1401-1404.
52. De Smet R, Van de Peer Y, (2012) Redundancy and rewiring of genetic networks following genome-wide duplication events. Current Opinion in Plant Biology 15: 168-176.
53. Baker CR, Hanson-Smith V, Johnson AD, (2013) Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science 342: 104-108.
54. Makino T, McLysaght A, (2010) Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proceedings of the National Academy of Sciences of the United States of America 107: 9270-9274.
55. Birchler JA, Veitia RA, (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. The New phytologist 186: 54-62.
56. Gout JF, Duret L, Kahn D, (2009) Differential retention of metabolic genes following whole-genome duplication. Molecular Biology and Evolution 26: 1067-1072.
57. Tang H, Woodhouse MR, Cheng F, Schnable JC, Pedersen BS, et al. (2012) Altered patterns of fractionation and exon deletions in brassica rapa support a two-step model of paleohexaploidy. Genetics 190: 1563-1574.
58. Sankoff D, Zheng C, Wang B, (2012) A model for biased fractionation after whole genome duplication. BMC Genomics 13: S8.
59. 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 Evolutionary Biology 9: 159.
60. Buggs R, Zhang L, Miles N, Tate J, Gao L, et al. (2011) Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Current Biology 21: 551-556.
61. Neyfakh AA, Baranova NN, Mizrokhi LJ, (2006) A system for studying evolution of life-like virtual organisms. Biology Direct 1: 23.