Genetica

, Volume 115, Issue 1, pp 37–47

Feast and famine in plant genomes

  • Jonathan F. Wendel
  • Richard C. Cronn
  • J. Spencer Johnston
  • H. James Price
Article

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.

cotton DNA content genome evolution genome size Gossypium Malvaceae molecular evolution 2C values 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant, Arabidopsis thaliana. Nature 408: 796-815.Google Scholar
  2. 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.Google Scholar
  3. Bennett, M.D., 1987. Variation in genomic form and its ecological implications. New Phytol. 106: 177-200.Google Scholar
  4. 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
  5. Bennett, M.D., A.V. Cox & I.J. Leitch, 1997. Angiosperm DNA cvalues database. http://www.rbgkew.org.uk/cval/database1.htmlGoogle Scholar
  6. Bennett, M.D. & I.J. Leitch, 1995. Nuclear DNA amounts in angiosperms. Ann. Bot. 76: 113-176.Google Scholar
  7. Bennett, M.D. & J.B. Smith, 1991. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. London B 334: 309-345.Google Scholar
  8. Bennetzen, J.L., 1996. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 4: 347-353.Google Scholar
  9. Bennetzen, J.L., 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42: 251-269.Google Scholar
  10. Bennetzen, J.L. & M. Freeling, 1997. The unified grass genome: synergy in synteny. Genome Res. 7: 301-306.Google Scholar
  11. Bennetzen, J.L. & E.A. Kellogg, 1997a. Do plants have a one-way ticket to genomic obesity? Plant Cell 9: 1509-1514.Google Scholar
  12. Bennetzen, J.L. & E.A. Kellogg, 1997b. Reply. Plant Cell 9: 1901-1902.Google Scholar
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. Deutsch, M. & M. Long, 1999. Intron-exon structure of eukaryotic model organisms. Nucl. Acids Res. 27: 3219-3228.Google Scholar
  19. Endrizzi, J.E., E.L. Turcotte & R.J. Kohel, 1985. Genetics, cytogenetics, and evolution of Gossypium. Adv. Genet. 23: 271-375.Google Scholar
  20. Farris, J.S., 1996. Parsimony jackknifing outperforms neighborjoining. Cladistics 12: 99-124.Google Scholar
  21. Federoff, N., 2000. Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. USA 97: 7002-7007.Google Scholar
  22. Fryxell, P.A., 1979. The Natural History of the Cotton Tribe. Texas A&M University Press, College Station, TX.Google Scholar
  23. Fryxell, P.A., 1992. A revised taxonomic interpretation of Gossypium L. (Malvaceae). Rheedea 2: 108-165.Google Scholar
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. Hughes, A.L. & M.K. Hughes, 1995. Small genomes for better flyers. Nature 377: 391.Google Scholar
  30. 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
  31. 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
  32. 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
  33. 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
  34. Kellogg, E.A., 1998. Relationships of cereal crops and other grasses. Proc. Natl. Acad. Sci. USA 95: 2005-2010.Google Scholar
  35. Kirik, A., S. Salomon & H. Puchta, 2000. Species-specific doublestrand break repair and genome evolution in plants. EMBO J. 2000: 5562-5566.Google Scholar
  36. LaDuke, J.C. & J.F. Doebley, 1995. A chloroplast DNA based phylogeny of the Malvaceae. Syst. Bot. 20: 259-271.Google Scholar
  37. 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
  38. Lagercrantz, U. & D.J. Lydiate, 1996. Comparative genome mapping in Brassica. Genetics 144: 1903-1910.Google Scholar
  39. Leitch, I.J. & M.D. Bennett, 1997. Polyploidy in angiosperms. Trends Plant Sci. 2: 470-476.Google Scholar
  40. 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
  41. 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
  42. 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
  43. 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
  44. Masterson, J., 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424.Google Scholar
  45. Miege, J. & N. Josserand, 1972. Nombres chromosomiques d'especes africaines et malgaches. Candollea 27: 283-292.Google Scholar
  46. Moore, G., K.M. Devos & Z. Wang, 1995. Grasses, line up and form a circle. Curr. Biol. 5: 737-739.Google Scholar
  47. 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
  48. 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
  49. 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
  50. 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
  51. Otto, S.P. & J. Whitton, 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437.Google Scholar
  52. 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
  53. Petrov, D.A., 1997. Slow but steady: reduction to genome size through biased mutation. Plant Cell 9: 1900-1901.Google Scholar
  54. Petrov, D.A., 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17: 23-28.Google Scholar
  55. 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
  56. Petrov, D.A., E.R. Lozovskaya & D.L. Hartl, 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384: 346-349.Google Scholar
  57. 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
  58. Polly, P.D., 2001. Paleontology and the comparative method: ancestral node reconstructions versus observed node values. Amer. Nat. 157: 596-609.Google Scholar
  59. Price, H.J., 1988. Nuclear DNA content variation within angiosperm species. Evol. Trends Plants 2: 53-60.Google Scholar
  60. Rabinowicz, P.D., 2000. Are obese plant genomes on a diet? Genome Res. 10: 893-894.Google Scholar
  61. 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
  62. 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
  63. 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
  64. 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
  65. Seelanan, T., A. Schnabel & J.F. Wendel, 1997. Congruence and consensus in the cotton tribe. Syst. Bot. 22: 259-290.Google Scholar
  66. 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
  67. 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
  68. Soltis, D.E. & P.S. Soltis, 1999. Polyploidy: origins of species and genome evolution. Trends Ecol. Evol. 9: 348-352.Google Scholar
  69. 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.Google Scholar
  70. Stace, C.A., 2000. Cytology and cytogenetics as a fundamental taxonomic resource for the 20th and 21st century. Taxon 49: 451-477.Google Scholar
  71. Swofford, D.L., 2001. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.Google Scholar
  72. Swofford, D.L. & W.P. Maddison, 1987. Reconstructing ancestral character states underWagner parsimony. Math. Biosci. 87: 199-229.Google Scholar
  73. Thomas, C.A., 1971. The genetic organisation of chromosomes. Annu. Rev. Genet. 5: 237-256.Google Scholar
  74. 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
  75. 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
  76. Vinogradov, A.E., 1999. Intron-genome size relationship on a large evolutionary scale. J. Mol. Evol. 49: 376-384.Google Scholar
  77. Vision, T.J., D.G. Brown & S.D. Tanksley, 2000. The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.Google Scholar
  78. Wendel, J.F., 2000. Genome evolution in polyploids. Plant Mol. Biol. 42: 225-249.Google Scholar
  79. 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
  80. 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
  81. Wessler, S.R., 1998. Transposable elements associated with normal plant genes. Physiol. Plantarum 103: 581-586.Google Scholar
  82. 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
  83. 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

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Jonathan F. Wendel
    • 1
  • Richard C. Cronn
    • 1
  • J. Spencer Johnston
    • 2
  • H. James Price
    • 3
  1. 1.Department of BotanyIowa State UniversityAmesUSA; (Phone
  2. 2.Department of EntomologyTexas A & M UniversityCollege StationUSA
  3. 3.Department of Soil and Crop SciencesTexas A & M UniversityCollege StationUSA

Personalised recommendations