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Copia-like retrotransposable element evolution in diploid and polyploid cotton (Gossypium L.)

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Summary

Copia-like retrotransposable elements were identified in allotetraploid cotton,Gossypium hirsutum, and two species representing its diploid progenitors,G. herbaceum andG. raimondii. These elements are present in high copy number in all three species. Because the two diploid genomic groups have been isolated on opposite sides of the world for 6–11 million years, horizontal transfer of elements between these species is highly unlikely. Elements were intensively sampled to generate a model ofcopia-like retrotransposable element evolution in systems where vertical transmission is the sole probable means of descent.Copia-like retrotransposon diversity is equally great in all threeGossypium species. Despite this high heterogeneity, analysis of 89 partial reverse transcriptase sequences resulted in the recognition of nine sharply differentiated retrotransposon lineages, each containing elements that share high sequence similarity. No evidence of horizontal transfer from other taxa was obtained. Phylogenetic analyses demonstrate that element topologies are incongruent withGossypium phylogeny. Consideration of processes that obscure phylogenetic reconstruction of multigene families (including sampling error, variable degrees of orthology and paralogy, differential lineage age and lineage loss and/or proliferation) demonstrates that incongruence between organismal and retrotransposon trees is expected under conditions in which vertical processes are the sole means of transmission. Identification of closely related elements between species allowed rates ofcopia-like retrotransposon sequence evolution to be estimated as approximately 10−9 nucleotide substitutions/site/year. These rates are consistent with the interpretation that these retrotransposons have been evolving under functional constraints for most of the time frame bracketed by the species studied. Extrapolation of these results to previous studies that sampled from more highly divergent taxa indicates that horizontal transfer need not be invoked to explain observed phylogenetic patterns.

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References

  • Abad PC, Vaury C, Pelisson A, Chaboissier M, Busseau I, Bucheton A (1989) A long interspersed repetitive element—the I factor ofDrosophila teissieri—is able to transpose in differentDrosophila species. Proc Natl Acad Sci USA 86:8887–8891

    CAS  PubMed  Google Scholar 

  • Appels R, Honeycutt RL (1986) rDNA: evolution over a billion years. In: Dutta SK (ed) DNA systematics, vol II. CRC Press, Boca Raton, FL, pp 81–135

    Google Scholar 

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer Associates, Sunderland, MA, pp 38–61

    Google Scholar 

  • Boeke JD, Garfinkel DJ, Styles CA, Fink GR (1985) Ty elements transpose through an RNA intermediate. Cell 40:491–500

    Article  CAS  PubMed  Google Scholar 

  • Boeke JD, Garfinkel DJ (1988) Yeast Ty elements as retroviruses. In: Koltin Y, Leibowitz MJ (eds) Viruses of fungi and simple eukaryotes. Marcel Dekker, New York pp 16–39

    Google Scholar 

  • Boeke JD (1989) Transposable elements inSaccharomyces cerevisiae. In: Berg DE, Howe MM (eds) Mobile DNA. Am Soc Microbiol, Washington, DC, pp 335–374

    Google Scholar 

  • Calvi BR, Hong TJ, Findley SD, Gelbart WM (1991) Evidence for a common evolutionary origin of inverted repeat transposons inDrosophila and plants:hobo, activator, and Tam 3. Cell 66:465–471

    Article  CAS  PubMed  Google Scholar 

  • Camirand A, Brisson N (1990) The complete nucleotide sequence of the Tst1 retrotransposon of potato. Nucleic Acids Res 18:4929

    CAS  PubMed  Google Scholar 

  • Daniels SB, Chovnick A, Boussy IA (1990a) Distribution ofhobo transposable elements in the genusDrosophila. Mol Biol Evol 7:589–606

    CAS  PubMed  Google Scholar 

  • Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990b) Evidence for horizontal transmission of the P transposable element betweenDrosophila species. Genetics 124:339–355

    CAS  PubMed  Google Scholar 

  • Demmin DS, Stockinger EJ, Chang YC, Walling LL (1989) Phylogenetic relationships between the chlorophyll a/b binding protein (CAB) multigene family: an intra- and interspecies study. J Mol Evol 29:266–279

    Article  CAS  PubMed  Google Scholar 

  • Devereux JP, Haeberli P, Smithies O (1984) A comprehensive set of sequence programs for the VAX. Nucleic Acids Res 12:387–395

    CAS  PubMed  Google Scholar 

  • Doolittle RF, Feng D-F, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Quart Rev Biol 64:1–30

    Article  CAS  PubMed  Google Scholar 

  • Doolittle RF, Feng D-F, Anderson KL, Alberro MR (1990) A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J Mol Evol 31:383–388

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ (1991) Evolution of higher-plant glutamine synthetase genes: tissue specificity as a criterion for predicting orthology. Mol Biol Evol 8:366–377

    CAS  Google Scholar 

  • Endrizzi JE, Turcotte EL, Kohel RJ (1985) Genetics, cytology and evolution ofGossypium. Adv Genet 23:271–375

    Article  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Article  CAS  PubMed  Google Scholar 

  • Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113

    Article  CAS  PubMed  Google Scholar 

  • Flavell AJ, Smith DB, Kumar A (1992a) Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet 231:233–242

    CAS  PubMed  Google Scholar 

  • Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A (1992b) Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res 20:3639–3644

    CAS  PubMed  Google Scholar 

  • Fourcade-Peronnet F, d'Auriol L, Becker J, Galibert F, Best-Belpomme M (1988) Primary structure and functional organization ofDrosophila 1731 retrotransposon. Nucleic Acids Res 16:6113–6125

    CAS  PubMed  Google Scholar 

  • Fryxell PA (1979) The natural history of the cotton tribe. Texas A&M Univ Press, College Station

    Google Scholar 

  • Galau GA, Wang HY-C, Hughes DW (1992) CottonMat5-A (C164) gene andMat5-D cDNAs encoding methionine rich 2S albumin storage proteins. Plant Physiol 99:779–782

    Article  CAS  PubMed  Google Scholar 

  • Geever RF, Katterman FRH, Endrizzi JE (1989) DNA hybridization analyses of aGossypium allotetraploid and two closely related diploid species. Theor Appl Genet 77:553–559

    Article  CAS  Google Scholar 

  • Gerbi SA (1985) Evolution of Ribosomal DNA. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 419–490

    Google Scholar 

  • Gibbs PEM, Strongin KB, McPherson A (1989) Evolution of legume seed storage proteins—a domain common to legumins and vicilins is duplicated in vicilins. Mol Biol Evol 6:614–623

    CAS  PubMed  Google Scholar 

  • Gojobori T, Moriyama EN, Kimura M (1990) Molecular clock of viral evolution, and the neutral theory. Proc Natl Acad Sci USA 87:10015–10018

    CAS  PubMed  Google Scholar 

  • Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

    Article  CAS  PubMed  Google Scholar 

  • Hirochika H, Fukuchi A, Kikuchi F (1992) Retrotransposon families in rice. Mol Gen Genet 233:209–216

    Article  CAS  PubMed  Google Scholar 

  • Houck MA, Clark JB, Peterson KR, Kidwell MG (1991) Possible horizontal transfer ofDrosophila genes by the miteProctolaelaps regalis. Science 253:1125–1129

    CAS  PubMed  Google Scholar 

  • Hu W-S, Temin HM (1990) Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc Natl Acad Sci USA 87:1556–1560

    CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of molecules in protein. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Katz RA, Skalka AM (1990) Generation of diversity in retroviruses. Annu Rev Genet 24:409–445

    Article  CAS  PubMed  Google Scholar 

  • Konieczny A., Voytas DF, Cummings MP, Ausubel FM (1991) A superfamily ofArabidopsis thaliana retrotransposons. Genetics 127:801–809

    CAS  PubMed  Google Scholar 

  • Maruyama K, Hartl D (1991) Evidence for interspecific transfer of the transposable elementmariner betweenDrosophila andZaprionus. J Mol Evol 33:514–524

    Article  CAS  PubMed  Google Scholar 

  • Martin SL, Voliva CF, Hardies SC, Edgell MH, Hutchison CA III (1985) Tempo and mode of concerted evolution in the L1 repeat family of mice. Mol Biol Evol 2:127–140

    CAS  PubMed  Google Scholar 

  • McClure MA, Johnson MS, Feng D-F, Doolittle RF (1988) Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85:2469–2473

    CAS  PubMed  Google Scholar 

  • Meagher RB (1991) Divergence and differential expression of actin gene families in higher plants. Int Rev Cytol 125:139–163

    Article  CAS  PubMed  Google Scholar 

  • Mizrokhi LJ, Mazo AM (1990) Evidence for horizontal transmission of the mobile elementjockey between distantdrosophila species. Proc Natl Acad Sci USA 87:9216–9220

    CAS  PubMed  Google Scholar 

  • Moore G, Lucas H, Batty N, Flavell RB (1991) A family of retrotransposons and associated genomic variation in wheat. Genomics 10:461–468

    Article  CAS  PubMed  Google Scholar 

  • Mount SM, Rubin GM (1985) Complete nucleotide sequence of theDrosophila transposable elementcopia: homology betweencopia and retroviral proteins. Mol Cell Biol 5:1630–1638

    CAS  PubMed  Google Scholar 

  • Munro HN, Fleck A (1966) The determination of nucleic acids. In: Glick D (ed) Methods of biochemical analysis, vol 14. John Wiley and Sons, New York, pp 113–176

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Rothnie HM, McCurrach KJ, Glover LA, Hardman N (1991) Retrotransposon-like nature of Tp1 elements: implications for the organization of highly repetitive, hypermethylated DNA in the genome ofPhysarum polycephalum. Nucleic Acids Res 19:279–286

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sambrook JE, Fritsch F, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sanderson MJ, Doyle JJ (1992) Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Syst Biol 41:4–17

    Google Scholar 

  • Sarkar G, Sommer SS (1990) Shedding light on PCR contamination. Nature 343:27

    Article  CAS  PubMed  Google Scholar 

  • Smyth DR (1991) Dispersed repeats in plant genomes. Chromosoma 100:355–359

    Article  Google Scholar 

  • Swofford DL (1991) PAUP: phylogenetic analysis using parsimony, version 3.0s. Computer program distributed by the Illinois Natural History Survey, Champaign, IL

  • Villemur R, Joyce CM, Haas NA, Goddard RH, Kopczak SD, Hussey PJ, Snustad DP, Silflow CD (1992) α-Tubulin gene family of maize (Zea mays L.): evidence for two ancient α-tubulin genes in plants. J Mol Biol 227:81–96

    Article  CAS  PubMed  Google Scholar 

  • Voytas DF, Ausubel FM (1988) Acopia-like transposable element family inArabidopsis thaliana. Nature 336:242–244

    Article  CAS  PubMed  Google Scholar 

  • Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992)copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128

    CAS  PubMed  Google Scholar 

  • Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci USA 86:4132–4136

    CAS  PubMed  Google Scholar 

  • Wendel JF, Albert VA (1992) Phylogenetics of the cotton genus (Gossypium L.): character-state weighted parsimony analysis of chloroplast DNA restriction site data and its systematic and biogeographic implications. Syst Bot 17:115–143

    Article  Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, Bessey Hall, Iowa State University, 50011, Ames, IA, USA

    Pamela L. VanderWiel & Jonathan F. Wendel

  2. Department of Zoology and Genetics, Iowa State University, 50011, Ames, IA, USA

    Daniel F. Voytas

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  1. Pamela L. VanderWiel
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  2. Daniel F. Voytas
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VanderWiel, P.L., Voytas, D.F. & Wendel, J.F. Copia-like retrotransposable element evolution in diploid and polyploid cotton (Gossypium L.). J Mol Evol 36, 429–447 (1993). https://doi.org/10.1007/BF02406720

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  • DOI: https://doi.org/10.1007/BF02406720

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