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Feast and famine in plant genomes

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Abstract

Plant genomes vary over several orders of magnitude in size, even among closely related species, yet the origin, genesis and significance of this variation are not clear. Because DNA content varies over a sevenfold range among diploid species in the cotton genus (Gossypium) and its allies, this group offers opportunities for exploring patterns and mechanisms of genome size evolution. For example, the question has been raised whether plant genomes have a ‘one-way ticket to genomic obesity’, as a consequence of retroelement accumulation. Few empirical studies directly address this possibility, although it is consistent with recent insights gleaned from evolutionary genomic investigations. We used a phylogenetic approach to evaluate the directionality of genome size evolution among Gossypium species and their relatives in the cotton tribe (Gossypieae, Malvaceae). Our results suggest that both DNA content increase and decrease have occurred repeatedly during evolution. In contrast to a model of unidirectional genome size change, the frequency of inferred genome size contraction exceeded that of expansion. In conjunction with other evidence, this finding highlights the dynamic nature of plant genome size evolution, and suggests that poorly understood genomic contraction mechanisms operate on a more extensive scale that previously recognized. Moreover, the research sets the stage for fine-scale analysis of the evolutionary dynamics and directionality of change for the full spectrum of genomic constituents.

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References

  • The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant, Arabidopsis thaliana. Nature 408: 796-815.

    Google Scholar 

  • Bennett, M.D., 1985. Intraspecific variation in DNA amount and the nucleotypic dimension in plant genetics, pp. 283-302 in Plant Genetics, edited by M. Freeling. A. R. Liss, NY.

  • Bennett, M.D., 1987. Variation in genomic form and its ecological implications. New Phytol. 106: 177-200.

    Google Scholar 

  • Bennett, M.D., P. Bhandol & I.J. Leitch, 2000. Nuclear DNA amounts in angiosperms and their modern uses-807 new estimates. Ann. Bot. 86: 859-909.

    Google Scholar 

  • Bennett, M.D., A.V. Cox & I.J. Leitch, 1997. Angiosperm DNA cvalues database. http://www.rbgkew.org.uk/cval/database1.html

  • Bennett, M.D. & I.J. Leitch, 1995. Nuclear DNA amounts in angiosperms. Ann. Bot. 76: 113-176.

    Google Scholar 

  • Bennett, M.D. & J.B. Smith, 1991. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. London B 334: 309-345.

    Google Scholar 

  • Bennetzen, J.L., 1996. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 4: 347-353.

    Google Scholar 

  • Bennetzen, J.L., 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42: 251-269.

    Google Scholar 

  • Bennetzen, J.L. & M. Freeling, 1997. The unified grass genome: synergy in synteny. Genome Res. 7: 301-306.

    Google Scholar 

  • Bennetzen, J.L. & E.A. Kellogg, 1997a. Do plants have a one-way ticket to genomic obesity? Plant Cell 9: 1509-1514.

    Google Scholar 

  • Bennetzen, J.L. & E.A. Kellogg, 1997b. Reply. Plant Cell 9: 1901-1902.

    Google Scholar 

  • Bensasson, D., D.A. Petrov, D.-X. Zhang, D.L. Hartl & G.M. Hewitt, 2001. Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol. Biol. Evol. 18: 246-253.

    Google Scholar 

  • Brubaker, C.L., A.H. Paterson & J.F. Wendel, 1999. Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42: 184-203.

    Google Scholar 

  • Cox, A.V., G.J. Abdelnour, M.D. Bennett & I.J. Leitch, 1998. Genome size and karyotype evolution in the slipper orchids (Cypripedioideae: Orchidaceae). Amer. J. Bot. 85: 681-687.

    Google Scholar 

  • Cronn, R., R.L. Small & J.F. Wendel, 1999. Duplicated genes evolve independently following polyploid formation in cotton. Proc. Natl. Acad. Sci. USA 96: 14406-14411.

    Google Scholar 

  • Cunningham, C.W., K.E. Omland & T.H. Oakley, 1998. Reconstructing ancestral character states: a critical reappraisal. Trends Ecol. Evol. 13: 361-366.

    Google Scholar 

  • Deutsch, M. & M. Long, 1999. Intron-exon structure of eukaryotic model organisms. Nucl. Acids Res. 27: 3219-3228.

    Google Scholar 

  • Endrizzi, J.E., E.L. Turcotte & R.J. Kohel, 1985. Genetics, cytogenetics, and evolution of Gossypium. Adv. Genet. 23: 271-375.

    Google Scholar 

  • Farris, J.S., 1996. Parsimony jackknifing outperforms neighborjoining. Cladistics 12: 99-124.

    Google Scholar 

  • Federoff, N., 2000. Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. USA 97: 7002-7007.

    Google Scholar 

  • Fryxell, P.A., 1979. The Natural History of the Cotton Tribe. Texas A&M University Press, College Station, TX.

    Google Scholar 

  • Fryxell, P.A., 1992. A revised taxonomic interpretation of Gossypium L. (Malvaceae). Rheedea 2: 108-165.

    Google Scholar 

  • Gaut, B.S. & J.F. Doebley, 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 94: 6808-6814.

    Google Scholar 

  • Gòmez, M.I., M.N. Islam-Faridi, M.S. Zwick, D.G. Czeschin, G.E. Hart, R.A. Wing, D.M. Stelly & H.J. Price, 1998. Tetraploid nature of Sorghum bicolor (L.) Moench. J. Hered. 89: 188-190.

    Google Scholar 

  • Grant, D., P. Cregan & R.C. Shoemaker, 2000. Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc. Natl. Acad. Sci. USA 97: 4168-4173.

    Google Scholar 

  • Gregory, T.R. & P.D.N. Hebert, 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9: 317-324.

    Google Scholar 

  • Hanson, R.E., M.N. Islam-Faridi, E.A. Percival, C.F. Crane, Y. Ji, T.D. McKnight, D.M. Stelly & H.J. Price, 1996. Distribution of 5S and 18S-28S rDNA loci in a tetraploid cotton (Gossypium hirsutum L.) and its putative diploid ancestors. Chromosoma 105: 55-61.

    Google Scholar 

  • Hughes, A.L. & M.K. Hughes, 1995. Small genomes for better flyers. Nature 377: 391.

    Google Scholar 

  • Jewell, D.C. & M.N. Islam-Faridi, 1994. Details of a technique for somatic chromosome preparation and C-banding of maize, pp. 484-493 in The Maize Handbook, edited by M. Freeling & V. Walbot. Springer, New York.

    Google Scholar 

  • Johnson, J.D., D.G. Higgins & T.J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673-4680.

    Google Scholar 

  • Johnston, J.S., M.D. Bennett, A.L. Rayburn, D.W. Galbraith & H.J. Price, 1999. Reference standards for determination of DNA content of plant nuclei. Amer. J. Bot. 86: 609-613.

    Google Scholar 

  • Kalendar, R., J. Tanskanen, S. Immonen, E. Nevo & A.H. Schulman, 2000. Genome evolution in wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA 97: 6603-6607.

    Google Scholar 

  • Kellogg, E.A., 1998. Relationships of cereal crops and other grasses. Proc. Natl. Acad. Sci. USA 95: 2005-2010.

    Google Scholar 

  • Kirik, A., S. Salomon & H. Puchta, 2000. Species-specific doublestrand break repair and genome evolution in plants. EMBO J. 2000: 5562-5566.

    Google Scholar 

  • LaDuke, J.C. & J.F. Doebley, 1995. A chloroplast DNA based phylogeny of the Malvaceae. Syst. Bot. 20: 259-271.

    Google Scholar 

  • Lagercrantz, U., 1998. Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent recombinations. Genetics 150: 1217-1228.

    Google Scholar 

  • Lagercrantz, U. & D.J. Lydiate, 1996. Comparative genome mapping in Brassica. Genetics 144: 1903-1910.

    Google Scholar 

  • Leitch, I.J. & M.D. Bennett, 1997. Polyploidy in angiosperms. Trends Plant Sci. 2: 470-476.

    Google Scholar 

  • Leitch, I.J., M.W. Chase & M.D. Bennett, 1998. Phylogenetic analysis of DNA C-values provides evidence for a small ancestral genome size in flowering plants. Ann. Bot. (suppl. A) 82: 85-94.

    Google Scholar 

  • Maddison, W.P., 1991. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Syst. Zool. 40: 304-314.

    Google Scholar 

  • Martins, E.P., 1999. COMPARE, Version 4.3. Computer Programs for the Statistical Analysis of Comparative Data. Distributed by the author via the WWW at http://darkwing.uoregon.edu/ ~compare4/. Department of Biology, University of Oregon, Eugene, Oregon.

    Google Scholar 

  • Martins, E.P. & T.F. Hansen, 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Amer. Nat. 149: 646-667.

    Google Scholar 

  • Masterson, J., 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424.

    Google Scholar 

  • Miege, J. & N. Josserand, 1972. Nombres chromosomiques d'especes africaines et malgaches. Candollea 27: 283-292.

    Google Scholar 

  • Moore, G., K.M. Devos & Z. Wang, 1995. Grasses, line up and form a circle. Curr. Biol. 5: 737-739.

    Google Scholar 

  • Moriyama, E.N., D.A. Petrov & D.L. Hartl, 1998. Genome size and intron size in Drosophila. Mol. Biol. Evol. 15: 770-773.

    Google Scholar 

  • Muravenko, O., A.R. Fedotov, E.O. Punina, L.I. Federova, V.G. Grif & A.V. Zelenin, 1998. Comparison of chromosome BrdUHoechst-Giemsa banding patterns of the A1 and (AD)2 genomes of cotton. Genome 41: 616-625.

    Google Scholar 

  • Oakley, T.H. & C.W. Cunningham, 2000. Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny. Evolution 54: 397-405.

    Google Scholar 

  • Ogata, H., W. Fujibuchi & M. Kanehisa, 1996. The size differences among mammalian introns are due to the accumulation of small deletions. FEBS Lett. 390: 99-103.

    Google Scholar 

  • Otto, S.P. & J. Whitton, 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437.

    Google Scholar 

  • Paterson, A.H., J.E. Bowers, M.D. Burow, X. Draye, C.G. Elsik, C.-X. Jiang, C.S. Katsar, Y.-R. Lan, R. Ming & R.J. Wright, 2000. Comparative genomics of plant chromosomes. Plant Cell 12: 1523-1539.

    Google Scholar 

  • Petrov, D.A., 1997. Slow but steady: reduction to genome size through biased mutation. Plant Cell 9: 1900-1901.

    Google Scholar 

  • Petrov, D.A., 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17: 23-28.

    Google Scholar 

  • Petrov, D.A. & D.L. Hartl, 1997. Trash DNA is what gets thrown away: high rate of DNA loss in Drosophila. Gene 205: 279-289.

    Google Scholar 

  • Petrov, D.A., E.R. Lozovskaya & D.L. Hartl, 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384: 346-349.

    Google Scholar 

  • Petrov, D.A., T.A. Sangster, J.S. Johnston, D.L. Hartl & K.L. Shaw, 2000. Evidence for DNA loss as a determinant of genome size. Science 287: 1060-1062.

    Google Scholar 

  • Polly, P.D., 2001. Paleontology and the comparative method: ancestral node reconstructions versus observed node values. Amer. Nat. 157: 596-609.

    Google Scholar 

  • Price, H.J., 1988. Nuclear DNA content variation within angiosperm species. Evol. Trends Plants 2: 53-60.

    Google Scholar 

  • Rabinowicz, P.D., 2000. Are obese plant genomes on a diet? Genome Res. 10: 893-894.

    Google Scholar 

  • Reinisch, A.J., J. Dong, C.L. Brubaker, D.M. Stelly, J.F. Wendel & A.H. Paterson, 1994. A detailed RFLP map of cotton, Gossypium hirsutum x G. barbadense: chromosome organization and evolution in a disomic polyploid genome. Genetics 138: 829-847.

    Google Scholar 

  • SanMiguel, P., B.S. Gaut, A. Tikhonov, Y. Nakajima & J.L. Bennetzen, 1998. The paleontology of intergene retrotransposons of maize: dating the strata. Nat. Gen. 20: 43-45.

    Google Scholar 

  • SanMiguel, P., A. Tikhonov, Y.K. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer, K.J. Edwards, M. Lee, Z. Avramova & J.L. Bennetzen, 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765-768.

    Google Scholar 

  • Seelanan, T., C.L. Brubaker, J.M. Stewart, L.A. Craven & J.F. Wendel, 1999. Molecular systematics of Australian Gossypium section Grandicalyx (Malvaceae). Syst. Bot. 24: 183-208.

    Google Scholar 

  • Seelanan, T., A. Schnabel & J.F. Wendel, 1997. Congruence and consensus in the cotton tribe. Syst. Bot. 22: 259-290.

    Google Scholar 

  • Shirasu, K., A.H. Schulman, T. Lahaye & P. Schulze-Lefert, 2000. A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 10: 908-915.

    Google Scholar 

  • Shoemaker, R.C., K. Polzin, J. Labate, J. Specht, E.C. Brummer, T. Olson, N. Young, V. Concibido, J. Wilcox, J.P. Tamulonis, G. Kochert & H.R. Boerma, 1996. Genome duplication in soybean (Glycine subgenus soja). Genetics 144: 329-338.

    Google Scholar 

  • Soltis, D.E. & P.S. Soltis, 1999. Polyploidy: origins of species and genome evolution. Trends Ecol. Evol. 9: 348-352.

    Google Scholar 

  • Sossey-Alaouni, K., H. Serieys, M. Tersac, P. Lambert, E. Schilling, Y. Griveau, F. Kaan & A. Bervill47-1, 1998. Evidence for several genomes in Helianthus. Theor. Appl. Genet. 97: 422-430.

  • Stace, C.A., 2000. Cytology and cytogenetics as a fundamental taxonomic resource for the 20th and 21st century. Taxon 49: 451-477.

    Google Scholar 

  • Swofford, D.L., 2001. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Swofford, D.L. & W.P. Maddison, 1987. Reconstructing ancestral character states underWagner parsimony. Math. Biosci. 87: 199-229.

    Google Scholar 

  • Thomas, C.A., 1971. The genetic organisation of chromosomes. Annu. Rev. Genet. 5: 237-256.

    Google Scholar 

  • Tikhonov, A., P. SanMiguel, Y. Nakajima, N.M. Gorenstein, J.L. Bennetzen & Z. Avramova, 1999. Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc. Natl. Acad. Sci. USA 96: 7409-7414.

    Google Scholar 

  • Vicient, C.M., A. Suoniemi, K. Anamthawat-Jonsson, J. Tanskanen, A. Beharav, N.E. & A.H. Schulman, 1999. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11: 1769-1784.

    Google Scholar 

  • Vinogradov, A.E., 1999. Intron-genome size relationship on a large evolutionary scale. J. Mol. Evol. 49: 376-384.

    Google Scholar 

  • Vision, T.J., D.G. Brown & S.D. Tanksley, 2000. The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.

    Google Scholar 

  • Wendel, J.F., 2000. Genome evolution in polyploids. Plant Mol. Biol. 42: 225-249.

    Google Scholar 

  • Wendel, J.F. & V.A. Albert, 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.

    Google Scholar 

  • Wendel, J.F., R.L. Small, R.C. Cronn & C.L. Brubaker, 1999. Genes, jeans, and genomes: reconstructing the history of cotton. Plant evolution in man-made habitats, pp. 133-161 in Proc. VIIth Int. Symp. Int. Org. Plant Biosystemat. Amsterdam.

    Google Scholar 

  • Wessler, S.R., 1998. Transposable elements associated with normal plant genes. Physiol. Plantarum 103: 581-586.

    Google Scholar 

  • Wessler, S.R., T.E. Bureau & S.E. White, 1995. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5: 814-821.

    Google Scholar 

  • Wilson, W.A., S.E. Harrington, W.L. Woodman, M. Lee, M.E. Sorrells & S.R. McCouch, 1999. Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated Panicoids. Genetics 153: 453-473.

    Google Scholar 

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Wendel, J.F., Cronn, R.C., Spencer Johnston, J. et al. Feast and famine in plant genomes. Genetica 115, 37–47 (2002). https://doi.org/10.1023/A:1016020030189

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