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Molecular Evidence for Asymmetric Evolution of Sister Duplicated Blocks after Cereal Polyploidy

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Abstract

Polyploidy (genome duplication) is thought to have contributed to the evolution of the eukaryotic genome, but complex genome structures and massive gene loss during evolution has complicated detection of these ancestral duplication events. The major factors determining the fate of duplicated genes are currently unclear, as are the processes by which duplicated genes evolve after polyploidy. Fine-scale analysis between homologous regions may allow us to better understand post-polyploidy evolution. Here, using gene-by-gene and gene-by-genome strategies, we identified the S5 region and four homologous regions within the japonica genome. Additional phylogenomic analyses of the comparable duplicated blocks indicate that four successive duplication events gave rise to these five regions, allowing us to propose a model for this local chromosomal evolution. According to this model, gene loss may play a major role in post-duplication genetic evolution at the segmental level. Moreover, we found molecular evidence that one of the sister duplicated blocks experienced more gene loss and a more rapid evolution subsequent to two recent duplication events. Given that these two recent duplication events were likely involved in polyploidy, this asymmetric evolution (gene loss and gene divergence) may be one possible mechanism accounting for the diploidization at the segmental level.

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Abbreviations

HR:

homologous region

DB:

duplicated block

JS5-BC:

japonica S5 BAC contig

References

  • E.D. Akhunov A.W. Goodyear S. Geng L.L. Qi B. Echalier et al. (2003) ArticleTitleThe organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms Genome Res. 13 753–763 Occurrence Handle10.1101/gr.808603 Occurrence Handle12695326

    Article  PubMed  Google Scholar 

  • J.L. Bennetzen C. Coleman R. Liu J. Ma W. Ramakrishna (2004) ArticleTitleConsistent over-estimation of gene number in complex plant genomes Curr. Opin. Plant Biol. 7 732–736 Occurrence Handle10.1016/j.pbi.2004.09.003 Occurrence Handle15491923

    Article  PubMed  Google Scholar 

  • J.L. Bennetzen J.X. Ma (2003) ArticleTitleThe genetic colinearity of rice and other cereals on the basis of genomic sequence analysis Curr. Opin. Plant Biol. 6 128–133 Occurrence Handle10.1016/S1369-5266(03)00015-3 Occurrence Handle12667868

    Article  PubMed  Google Scholar 

  • G. Blanc A. Barakat R. Guyot R. Cooke M. Delseny (2000) ArticleTitleExtensive duplication and reshuffling in the Arabidopsis genome Plant Cell 12 1093–1101 Occurrence Handle10.1105/tpc.12.7.1093 Occurrence Handle10899976

    Article  PubMed  Google Scholar 

  • G. Blanc K. Hokamp K.H. Wolfe (2003) ArticleTitleA recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome Genome Res. 13 137–144 Occurrence Handle10.1101/gr.751803 Occurrence Handle12566392

    Article  PubMed  Google Scholar 

  • G. Blanc K.H. Wolfe (2004) ArticleTitleFunctional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution Plant Cell 16 1679–1691 Occurrence Handle10.1105/tpc.021410 Occurrence Handle15208398

    Article  PubMed  Google Scholar 

  • J.E. Bowers B.A. Chapman J.K. Rong A.H. Paterson (2003) ArticleTitleUnravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events Nature 422 433–438 Occurrence Handle10.1038/nature01521 Occurrence Handle12660784

    Article  PubMed  Google Scholar 

  • L Comai A.P. Tyagi K. Winter R. Holmes-Davis S.H. Reynolds et al. (2000) ArticleTitlePhenotypic instability and rapid gene silencing in newly formed arabidopsis allotetraploids Plant Cell 12 1551–1568 Occurrence Handle10.1105/tpc.12.9.1551 Occurrence Handle11006331

    Article  PubMed  Google Scholar 

  • G.C. Conant A. Wagner (2003) ArticleTitleAsymmetric sequence divergence of duplicate genes Genome Res. 13 2052–2058 Occurrence Handle10.1101/gr.1252603 Occurrence Handle12952876

    Article  PubMed  Google Scholar 

  • M. Delseny (2003) ArticleTitleTowards an accurate sequence of the rice genome Cure. Opin. Plant Biol. 6 101–105 Occurrence Handle10.1016/S1369-5266(03)00010-4

    Article  Google Scholar 

  • F.S. Dietrich S. Voegeli S. Brachat A. Lerch K. Gates et al. (2004) ArticleTitleThe Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome Science 304 304–307 Occurrence Handle10.1126/science.1095781 Occurrence Handle15001715

    Article  PubMed  Google Scholar 

  • B. Dujon D. Sherman G. Fischer P. Durrens S. Casaregola et al. (2004) ArticleTitleGenome evolution in yeasts Nature 430 35–44 Occurrence Handle10.1038/nature02579 Occurrence Handle15229592

    Article  PubMed  Google Scholar 

  • M.D. Ermolaeva M. Wu J.A. Eisen S.L. Salzberg (2003) ArticleTitleThe age of the Arabidopsis thaliana genome duplication Plant Mol. Biol. 51 859–866 Occurrence Handle10.1023/A:1023001130337 Occurrence Handle12777046

    Article  PubMed  Google Scholar 

  • Q. Feng Y.J. Zhang P. Hao S.Y. Wang G. Fu et al. (2002) ArticleTitleSequence and analysis of rice chromosome 4 Nature 420 316–320 Occurrence Handle10.1038/nature01183 Occurrence Handle12447439

    Article  PubMed  Google Scholar 

  • A. Force M. Lynch F.B. Pickett A. Amores Y.L. Yan et al. (1999) ArticleTitlePreservation of duplicate genes by complementary, degenerative mutations Genetics 151 1531–1545 Occurrence Handle10101175

    PubMed  Google Scholar 

  • B.S. Gaut B.R. Morton B.C. McCaig M.T. Clegg (1996) ArticleTitleSubstitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL Proc. Natl. Acad. Sci. USA 93 10274–10279 Occurrence Handle10.1073/pnas.93.19.10274 Occurrence Handle8816790

    Article  PubMed  Google Scholar 

  • S.A. Goff D. Ricke T.H. Lan G. Presting R.L. Wang et al. (2002) ArticleTitleA draft sequence of the rice genome (Oryza sativa L. ssp. japonica) Science 296 92–100 Occurrence Handle10.1126/science.1068275 Occurrence Handle11935018

    Article  PubMed  Google Scholar 

  • X. Gu Y.F. Wang J.Y. Gu (2002) ArticleTitleAge distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution Nature Genet. 31 205–209 Occurrence Handle10.1038/ng902 Occurrence Handle12032571

    Article  PubMed  Google Scholar 

  • Haas, B.J., Volfovsky, N., Town, C.D., Troukhan, M., Alexandrov N. et al. 2002. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol. 3: RESEARCH0029

  • T.A. Hall (1999) ArticleTitleBioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucl. Acids Symp. Ser. 41 95–98

    Google Scholar 

  • Ikehashi, H., Araki, H. 1986. Genetics of F1 sterility in remote crosses of rice. In Rice Genetics, IRRI, Manila Philippines, pp. 119–130

  • K. Kashkush M. Feldman A.A. Levy (2002) ArticleTitleGene loss, silencing and activation in a newly synthesized wheat allotetraploid Genetics 160 1651–1659 Occurrence Handle11973318

    PubMed  Google Scholar 

  • M. Kellis B.W. Birren E.S. Lander (2004) ArticleTitleProof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae Nature 428 617–624 Occurrence Handle10.1038/nature02424 Occurrence Handle15004568

    Article  PubMed  Google Scholar 

  • S. Kikuchi K. Satoh T. Nagata N. Kawagashira K. Doi et al. (2003) ArticleTitleCollection, mapping, and annotation of over 28,000 cDNA clones from japonica rice Science 301 376–379 Occurrence Handle10.1126/science.1081288 Occurrence Handle12869764

    Article  PubMed  Google Scholar 

  • H.-M. Ku T. Vision J. Liu S.D. Tanksley (2000) ArticleTitleComparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny Proc. Natl. Acad. Sci. USA 97 9121–9126 Occurrence Handle10.1073/pnas.160271297 Occurrence Handle10908680

    Article  PubMed  Google Scholar 

  • S. Kumar K. Tamura I.B. Jakobsen M. Nei (2001) ArticleTitleMEGA2: molecular evolutionary genetics analysis software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle11751241

    Article  PubMed  Google Scholar 

  • J. Lai J. Ma Z. Swigonova W. Ramakrishna E. Linton et al. (2004) ArticleTitleGene loss and movement in the maize genome Genome Res 14 1924–1931 Occurrence Handle10.1101/gr.2701104 Occurrence Handle15466290

    Article  PubMed  Google Scholar 

  • L.J. Leitch M.D. Bennett (1997) ArticleTitlePolyploidy in angiosperms Trends Plant Sci. 2 470–476 Occurrence Handle10.1016/S1360-1385(97)01154-0

    Article  Google Scholar 

  • A.A. Levy M. Feldman (2002) ArticleTitleThe impact of polyploidy on grass genome evolution Plant Physiol. 130 1587–1593 Occurrence Handle10.1104/pp.015727 Occurrence Handle12481041

    Article  PubMed  Google Scholar 

  • W.H. Li (1993) ArticleTitleUnbiased estimation of the rates of synonymous and nonsynonymous substitution J. Mol. Evol. 36 96–99 Occurrence Handle8433381

    PubMed  Google Scholar 

  • H. Liu R. Sachidanandam L. Stein (2001) ArticleTitleComparative genomics between rice and Arabidopsis shows scant collinearity in gene order Genome Res. 11 2020–2026 Occurrence Handle10.1101/gr.194501 Occurrence Handle11731491

    Article  PubMed  Google Scholar 

  • K.D. Liu J. Wang H.B. Liu C.G. Xu A.M. Liu et al. (1997) ArticleTitleA genome-wide analysis of wide compatibility in rice and the precise location of the S5 locus in the molecular map Theor. Appl. Genet. 95 809–814 Occurrence Handle10.1007/s001220050629

    Article  Google Scholar 

  • M. Lynch J.S. Conery (2000) ArticleTitleThe evolutionary fate and consequences of duplicate genes Science 290 1151–1155 Occurrence Handle10.1126/science.290.5494.1151 Occurrence Handle11073452

    Article  PubMed  Google Scholar 

  • J. Masterson (1994) ArticleTitleStomatal size in fossil plants: evidence for polyploidy in majority of angiosperms Science 264 421–424

    Google Scholar 

  • A. McLysaght K. Hokamp K.H. Wolfe (2002) ArticleTitleExtensive genomic duplication during early chordate evolution Nature Genet. 31 200–204 Occurrence Handle10.1038/ng884 Occurrence Handle12032567

    Article  PubMed  Google Scholar 

  • M. Nei T. Gojobori (1986) ArticleTitleSimple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions Mol. Biol. Evol. 3 418–426 Occurrence Handle3444411

    PubMed  Google Scholar 

  • S. Ohen (1970) Evolution by Gene Duplication George Allen and Unwin London, UK

    Google Scholar 

  • H. Ozkan A.A. Levy M. Feldman (2001) ArticleTitleAllopolyploidy-Induced Rapid Genome Evolution in the Wheat (Aegilops-Triticum) Group Plant Cell 13 1735–1747 Occurrence Handle10.1105/tpc.13.8.1735 Occurrence Handle11487689

    Article  PubMed  Google Scholar 

  • A.H. Paterson J.E. Bowers B.A. Chapman (2004) ArticleTitleAncient polyploidization predating divergence of the cereals, and its consequences for comparative genomics Proc. Natl Acad. Sci. USA 101 9903–9908 Occurrence Handle10.1073/pnas.0307901101 Occurrence Handle15161969

    Article  PubMed  Google Scholar 

  • T. Sasaki T. Matsumoto K. Yamamoto K. Sakata T. Baba et al. (2002) ArticleTitleThe genome sequence and structure of rice chromosome 1 Nature 420 312–316 Occurrence Handle10.1038/nature01184 Occurrence Handle12447438

    Article  PubMed  Google Scholar 

  • C. Seoighe (2003) ArticleTitleTurning the clock back on ancient genome duplication Curr. Opin. Genet. Dev. 13 636–643 Occurrence Handle10.1016/j.gde.2003.10.005 Occurrence Handle14638327

    Article  PubMed  Google Scholar 

  • H. Shaked K. Kashkush H. Ozkan M. Feldman A.A. Levy (2001) ArticleTitleSequence Elimination and-Cytosine Methylation Are Rapid and Reproducible Responses of the Genome to Wide Hybridization and Allopolyploidy in Wheat Plant Cell 13 1749–1759 Occurrence Handle10.1105/tpc.13.8.1749 Occurrence Handle11487690

    Article  PubMed  Google Scholar 

  • C. Simillion K. Vandepoele M.C.E. Montagu M. Zabeau Y. Peer ParticleVan de (2002) ArticleTitleThe hidden duplication past of Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 99 13627–13632 Occurrence Handle10.1073/pnas.212522399 Occurrence Handle12374856

    Article  PubMed  Google Scholar 

  • K. Song P. Lu K. Tang T.C. Osborn (1995) ArticleTitleRapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution Proc. Natl. Acad. Sci. USA 92 7719–7723 Occurrence Handle7644483

    PubMed  Google Scholar 

  • F. Tajima (1993) ArticleTitleSimple methods for testing the molecular evolutionary clock hypothesis Genetics 135 599–607 Occurrence Handle8244016

    PubMed  Google Scholar 

  • Y. Peer ParticleVan de J.S. Taylor I. Braasch A. Meyer (2001) ArticleTitleThe ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes J. Mol. Evol. 53 436–446 Occurrence Handle10.1007/s002390010233 Occurrence Handle11675603

    Article  PubMed  Google Scholar 

  • K. Vandepoele Y. Saeys C. Simillion J. Raes Y. Peer ParticleVan de (2002) ArticleTitleThe automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice Genome Res. 12 1792–1801 Occurrence Handle10.1101/gr.400202 Occurrence Handle12421767

    Article  PubMed  Google Scholar 

  • K. Vandepoele C. Simillion ParticleVan de Y. Peer (2003) ArticleTitleEvidence that rice and other cereals are ancient aneuploids Plant Cell 15 2192–2202 Occurrence Handle10.1105/tpc.014019 Occurrence Handle12953120

    Article  PubMed  Google Scholar 

  • T.J. Vision D.G. Brown S.D. Tanksley (2000) ArticleTitleThe origins of genomic duplications in Arabidopsis Science 290 2114–2117 Occurrence Handle10.1126/science.290.5499.2114 Occurrence Handle11118139

    Article  PubMed  Google Scholar 

  • H.B. Wang B. Liu H.F. Yi Y. Fan L.S. Liu et al. (2002) ArticleTitleIdentification and sequence analysis of a new clone R2I19 in rice (Oryza sativa L.) S5 locus Acta Scientiarum Naturalium Uniersitatis Sunyatseni 41 78–82

    Google Scholar 

  • K.H. Wolfe (2001) ArticleTitleYesterday’s polyploids and the mystery of diploidization Nat. Rev. Genet. 2 333–341 Occurrence Handle10.1038/35072009 Occurrence Handle11331899

    Article  PubMed  Google Scholar 

  • K.H. Wolfe D.C. Shields (1997) ArticleTitleMolecular evidence for an ancient duplication of the entire yeast genome Nature 387 708–713 Occurrence Handle10.1038/42711 Occurrence Handle9192896

    Article  PubMed  Google Scholar 

  • X. Xia Z. Xie (2001) ArticleTitleDAMBE: Software package for data analysis in molecular biology and evolution Journal of Heredity 92 371–373 Occurrence Handle10.1093/jhered/92.4.371 Occurrence Handle11535656

    Article  PubMed  Google Scholar 

  • Z. Yang (1997) ArticleTitlePAML: a program package for phylogenetic analysis by maximum likelihood Comput. Appl. Biosci. 13 555–556 Occurrence Handle9367129

    PubMed  Google Scholar 

  • Z. Yang R. Nielsen (2000) ArticleTitleEstimating synonymous and nonsynonymous substitution rates under realistic evolutionary models Mol. Biol. Evol. 17 32–43 Occurrence Handle10666704

    PubMed  Google Scholar 

  • J. Yu S.N. Hu J. Wang G.K.S. Wong S.G. Li et al. (2002) ArticleTitleA draft sequence of the rice genome (Oryza sativa L. ssp. indica) Science 296 79–92 Occurrence Handle10.1126/science.1068037 Occurrence Handle11935017

    Article  PubMed  Google Scholar 

  • Y.S. Yu T. Rambo J. Currie C. Saski H.R. Kim et al. (2003) ArticleTitleIn-depth view of structure, activity, and evolution of rice chromosome 10 Science 300 1566–1569 Occurrence Handle10.1126/science.1083523 Occurrence Handle12791992

    Article  PubMed  Google Scholar 

  • Z. Zhang H. Kishino (2004) ArticleTitleGenomic background predicts the fate of duplicated genes: evidence from the yeast genome Genetics 166 1995–1999 Occurrence Handle10.1534/genetics.166.4.1995 Occurrence Handle15126414

    Article  PubMed  Google Scholar 

  • P.A. Ziolkowski G. Blanc J. Sadowski (2003) ArticleTitleStructural divergence of chromosomal segments that arose from successive duplication events in the Arabidopsis genome Nucleic Acids Res. 31 1339–1350 Occurrence Handle10.1093/nar/gkg201 Occurrence Handle12582254

    Article  PubMed  Google Scholar 

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Correspondence to Jinfa Wang.

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Wang, H., Yu, L., Lai, F. et al. Molecular Evidence for Asymmetric Evolution of Sister Duplicated Blocks after Cereal Polyploidy. Plant Mol Biol 59, 63–74 (2005). https://doi.org/10.1007/s11103-005-4414-1

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