Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants

Plant Physiology

Volumn 161, Issue 4, 2013, Pages 1844-1861

  Jiang, Wen Kai ^a,b   Liu, Yun Long ^b,c,d   Xia, En Hua ^b,c,d   Gao, Li Zhi ^b  

^a Germplasm Bank of Wild Species in Southwest China   (China)

^b Plant Germplasm and Genomics Center Germplasm Bank of Wild Species   (China)

^c KUNMING INSTITUTE OF BOTANY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84875732837     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.200147     Document Type: Article

References (97)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Amoutzias GD, He Y, Gordon J, Mossialos D, Oliver SG, Van de Peer Y (2010) Posttranslational regulation impacts the fate of duplicated genes. Proc Natl Acad Sci USA 107: 2967-2971.
3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29.
4. Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Ségurens B, Daubin V, Anthouard V, Aiach N, et al (2006) Global trends of wholegenome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171-178.
5. Barker MS, Kane NC, Matvienko M, Kozik A, Michelmore RW, Knapp SJ, Rieseberg LH (2008) Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25: 2445-2455.
6. Benovoy D, Morris RT, Morin A, Drouin G (2005) Ectopic gene conversions increase the G + C content of duplicated yeast and Arabidopsis genes. Mol Biol Evol 22: 1865-1868.
7. Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19: 395-402.
8. Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186: 54-62.
9. Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000) Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12: 1093-1101.
10. Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13: 137-144.
11. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16: 1679-1691.
12. Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
13. Brunet FG, Roest Crollius H, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23: 1808-1816.
14. Chapman BA, Bowers JE, Feltus FA, Paterson AH (2006) Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication. Proc Natl Acad Sci USA 103: 2730-2735.
15. Conant GC, Wolfe KH (2007) Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol Syst Biol 3: 129.
16. Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, et al (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16: 738-749.
17. Davis JC, Petrov DA (2004) Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biol 2: E55.
18. Davis JC, Petrov DA (2005) Do disparate mechanisms of duplication add similar genes to the genome? Trends Genet 21: 548-551.
19. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314.
20. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42: 443-461.
21. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
22. Freeling M (2008) The evolutionary position of subfunctionalization, downgraded. Genome Dyn 4: 25-40.
23. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60: 433-453.
24. Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16: 805-814.
25. Gao LZ, Innan H (2004) Very low gene duplication rate in the yeast genome. Science 306: 1367-1370.
26. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy: analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
27. Gibson TJ, Spring J (1998) Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multidomain proteins. Trends Genet 14: 46-49.
28. discussion 49-50.
29. Gout JF, Kahn D, Duret L (2010) The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genet 6: e1000944.
30. Guan Y, Dunham MJ, Troyanskaya OG (2007) Functional analysis of gene duplications in Saccharomyces cerevisiae. Genetics 175: 933-943.
31. Haas BJ, Delcher AL, Wortman JR, Salzberg SL (2004) DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20: 3643-3646.
32. 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 Biol 8: R209.
33. Hartigan J, Wong M (1979) Algorithm AS136: a k-means clustering algorithm. Appl Stat 28: 100-108.
34. He X, Zhang J (2005) Gene complexity and gene duplicability. Curr Biol 15: 1016-1021.
35. He X, Zhang J (2006) Higher duplicability of less important genes in yeast genomes. Mol Biol Evol 23: 144-151.
36. Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L, et al (2009) Ensembl 2009. Nucleic Acids Res 37: D690-D697.
37. Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
38. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
39. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957.
40. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
41. Jin L, Kryukov K, Clemente JC, Komiyama T, Suzuki Y, Imanishi T, Ikeo K, Gojobori T (2008) The evolutionary relationship between gene duplication and alternative splicing. Gene 427: 19-31.
42. Kassahn KS, Dang VT, Wilkins SJ, Perkins AC, Ragan MA (2009) Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Res 19: 1404-1418.
43. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
44. Kimura M, King JL (1979) Fixation of a deleterious allele at one of two "duplicate" loci by mutation pressure and random drift. Proc Natl Acad Sci USA 76: 2858-2861.
45. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV (2002) Selection in the evolution of gene duplications. Genome Biol 3: RESEARCH0008.
46. Kopelman NM, Lancet D, Yanai I (2005) Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 37: 588-589.
47. Li L, Huang Y, Xia X, Sun Z (2006) Preferential duplication in the sparse part of yeast protein interaction network. Mol Biol Evol 23: 2467-2473.
48. Liang H, Li WH (2007) Gene essentiality, gene duplicability and protein connectivity in human and mouse. Trends Genet 23: 375-378.
49. Liang H, Plazonic KR, Chen J, Li WH, Fernández A (2008) Protein underwrapping causes dosage sensitivity and decreases gene duplicability. PLoS Genet 4: e11.
50. Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140: 336-348.
51. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
52. Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3: 35-44.
53. Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
54. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102: 5454-5459.
55. Ohno S (1970) Evolution by Gene Duplication. Springer-Verlag, Berlin
56. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34: 401-437.
57. Pál C, Papp B, Lercher MJ (2006) An integrated view of protein evolution. Nat Rev Genet 7: 337-348.
58. Papp B, Pál C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
59. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
60. Paterson AH, Bowers JE, Burow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming R, et al (2000) Comparative genomics of plant chromosomes. Plant Cell 12: 1523-1540.
61. Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101: 9903-9908.
62. Paterson AH, Chapman BA, Kissinger JC, Bowers JE, Feltus FA, Estill JC (2006) Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22: 597-602.
63. Prachumwat A, Li WH (2006) Protein function, connectivity, and duplicability in yeast. Mol Biol Evol 23: 30-39.
64. Prufer K, Muetzel B, Do HH, Weiss G, Khaitovich P, Rahm E, Paabo S, Lachmann M, Enard W (2007) FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinformatics 8: 41.
65. Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, Strauss SH, Brunner AM, Difazio SP (2012) Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res 22: 95-105.
66. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14: 1163-1175.
67. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506.
68. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
69. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
70. Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17: 505-512.
71. Sémon M, Wolfe KH (2008) Preferential subfunctionalization of slowevolving genes after allopolyploidization in Xenopus laevis. Proc Natl Acad Sci USA 105: 8333-8338.
72. Seoighe C, Gehring C (2004) Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet 20: 461-464.
73. Seoighe C, Wolfe KH (1999) Yeast genome evolution in the post-genome era. Curr Opin Microbiol 2: 548-554.
74. Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, et al (2010) RNA-Seq atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10: 160.
75. Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13: 1749-1759.
76. Simillion C, Vandepoele K, Van Montagu MCE, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99: 13627-13632.
77. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng CF, Sankoff D, Depamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96: 336-348.
78. Su ZX, Wang J, Yu J, Huang XQ, Gu X (2006) Evolution of alternative splicing after gene duplication. Genome Res 16: 182-189.
79. Sugino RP, Innan H (2006) Selection for more of the same product as a force to enhance concerted evolution of duplicated genes. Trends Genet 22: 642-644.
80. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34: W609-W612.
81. Swigonová Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14: 1916-1923.
82. Talavera D, Vogel C, Orozco M, Teichmann SA, de la Cruz X (2007) The (in)dependence of alternative splicing and gene duplication. PLoS Comput Biol 3: 375-388.
83. Tang H, Bowers JE, Wang X, Paterson AH (2010) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA 107: 472-477.
84. Tatarinova TV, Alexandrov NN, Bouck JB, Feldmann KA (2010) GC3 biology in corn, rice, sorghum and other grasses. BMC Genomics 11: 308.
85. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
86. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
87. Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.
88. Walsh JB (1995) How often do duplicated genes evolve new functions? Genetics 139: 421-428.
89. Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, et al (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61: 752-766.
90. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42: 225-249.
91. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149: 981-993.
92. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106: 13875-13879.
93. Wu X, Qi X (2010) Genes encoding hub and bottleneck enzymes of the Arabidopsis metabolic network preferentially retain homeologs through whole genome duplication. BMC Evol Biol 10: 145.
94. Wu Y, Zhu Z, Ma L, Chen M (2008) The preferential retention of starch synthesis genes reveals the impact of whole-genome duplication on grass evolution. Mol Biol Evol 25: 1003-1006.
95. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, Bar-Even A, Horn-Saban S, Safran M, Domany E, et al (2005) Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21: 650-659.
96. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
97. Zhang JZ, Nielsen R, Yang ZH (2005) Evaluation of an improved branchsite likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472-2479