title: Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years.
abstract: Analyses of selected bacterial artificial chromosomes (BACs) clones suggest that the retrotransposon component of angiosperm genomes can be amplified or deleted, leading to genome turnover. Here, Nicotiana allopolyploids were used to characterize the nature of sequence turnover across the whole genome in allopolyploids known to be of different ages. Using molecular-clock analyses, the likely age of Nicotiana allopolyploids was estimated. Genomic in situ hybridization (GISH) and tandem repeat characterization were used to determine how the parental genomic compartments of these allopolyploids have diverged over time. Paternal genome sequence losses, retroelement activity and intergenomic translocation have been reported in early Nicotiana tabacum evolution (up to 200,000 yr divergence). Here it is shown that within 1 million years of allopolyploid divergence there is considerable exchange of repeats between parental chromosome sets. After c. 5 million years of divergence GISH fails. This GISH failure may represent near-complete genome turnover, probably involving the replacement of nongenic sequences with new, or previously rare sequence types, all occurring within a conserved karyotype structure. This mode of evolution may influence or be influenced by long-term diploidization processes that characterize angiosperm polyploidy-diploid evolutionary cycles.
authors: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK.
authors: K Yoong
authors: KY
authors: Lim
authors: Institute of Biophysics Academy of Sciences of the Czech Republic, CZ-61265 Brno, Czech Republic.
authors: Ales
authors: A
authors: Kovarik
authors: Institute of Biophysics Academy of Sciences of the Czech Republic, CZ-61265 Brno, Czech Republic.
authors: Roman
authors: R
authors: Matyasek
authors: Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3DS, UK.
authors: Mark W
authors: MW
authors: Chase
authors: Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3DS, UK.
authors: James J
authors: JJ
authors: Clarkson
authors: Laboratoire de Biologie Cellulaire, INRA - Centre de Versailles, F-78026 Versailles, France.
authors: M A
authors: MA
authors: Grandbastien
authors: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK.
authors: Andrew R
authors: AR
authors: Leitch
mesh_terms: D005075:Biological Evolution; D032461:Chromosomes, Plant; D018745:Genome, Plant / Q000235:genetics*; D017404:In Situ Hybridization, Fluorescence; D007621:Karyotyping; D011123:Polyploidy; D013997:Time Factors; D014026:Nicotiana / Q000235:genetics*
references: Abbott RJ, Lowe AJ. 2004. Origins, establishment and evolution of two new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles. Biological Journal of the Linnean Society 82: 467-474.
references: Adams KL, Wendel JF. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135-141.
references: Adams KL, Percifield R, Wendel JF. 2004. Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168: 2217-2226.
references: Ainouche ML, Baumel A, Salmon A. 2004. Spartina anglica C.E. Hubbard: a natural model system for studying early evolutionary changes that affect allopolyploid genomes. Biological Journal of the Linnean Society 82: 475-484.
references: Baldini A, Miller DA, Miller OJ, Ryder OA, Mitchell AR. 1991. A chimpanzee-derived chromosome-specific alpha-satellite DNA-sequence conserved between chimpanzee and human. Chromosoma 100: 156-161.
references: Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A. 2005. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343-360.
references: Burk LG. 1973. Partial self-fertility in a theoretical amphiploid progenitor of N. tabacum. Journal of Heredity 64: 348-350.
references: Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS. 2003. Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Annals of Botany 92: 107-127.
references: Clarkson J. 2006. Nicotiana (Solanaceae): Insights from molecular phylogenetics and cytogenetics. PhD Thesis. London, UK: Queen Mary University of London.
references: Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW. 2004. Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Molecular Phylogenetics and Evolution 33: 75-90.
references: Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR. 2005. Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytologist 168: 241-252.
references: Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846.
references: Dadejová M, Lim KY, Soucková-Skalická K, Matyásek R, Grandbastien MA, Leitch AR, Kovarik A. 2007. Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytologist 174: 658-668.
references: Dawe RK. 2005. Centromere renewal and replacement in the plant kingdom. Proceedings of the National Academy of Sciences, USA 102: 11573-11574.
references: Gill BS. 1991. Nucleocytoplasmic interaction (NCI) hypothesis of genome evolution and speciation in polyploid plants. In: Sasakuma T, Kinoshita T, eds. Proceedings Of the Kihara Memorial International Symposium on Cytoplasmic Engineering in Wheat. Yokohama, Japan: Kihara Memorial Foundation, 48-53.
references: Gill BS, Friebe B. 1998. Plant cytogenetics at the dawn of the 21st century. Current Opinion in Plant Biology 1: 109-115.
references: Glazko GV, Nei M. 2003. Estimation of divergence times for major lineages of primate species. Molecular Biology and Evolution 20: 424-434.
references: Goodspeed TH. 1954. The genus Nicotiana. Waltham, MA, USA: Chronica Botanica Company.
references: Hall SE, Luo S, Hall AE, Preuss D. 2005. Differential rates of local and global homogenization in centromere satellites from Arabidopsis relatives. Genetics 170: 1913-1927.
references: Kashkush K, Feldman M, Levy AA. 2002. Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160: 1651-1659.
references: Kashkush K, Feldman M, Levy AA. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genetics 33: 102-106.
references: Knapp S, Chase MW, Clarkson JJ. 2004. Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53: 73-82.
references: Koukalova B, Konarnitsky IK, Kuhrova V. 1993. The distribution of tobacco HRS60 DNA repeated sequences in species of the genus Nicotiana. Plant Sciences 99: 39-44.
references: Kovarik A, Matyasek R, Lim KY, Skalicka K, Koukalova B, Knapp S, Chase MW, Leitch AR. 2004. Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biological Journal of the Linnean Society 82: 615-625.
references: Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyasek R, Rocca J, Soltis DE, Soltis PS. 2005. Rapid concerted evolution of nuclear ribosomal DNA in two tragopogon allopolyploids of recent and recurrent origin. Genetics 169: 931-944.
references: Lim KY, Matyasek R, Lichtenstein CP, Leitch AR. 2000. Molecular cytogenetic analyses and phylogenetic studies in the Nicotiana section Tomentosae. Chromosoma 109: 245-258.
references: Lim KY, Matyasek R, Kovarik A, Leitch AR. 2004. Genome evolution in allotetraploid Nicotiana. Biological Journal of the Linnean Society 82: 599-606.
references: Lim KY, Matyasek R, Kovarik A, Fulnecek J, Leitch AR. 2005. Molecular cytogenetics and tandem repeat sequence evolution in the allopolyploid Nicotiana rustica compared with diploid progenitors N. paniculata and N. undulata. Cytogenetic and Genome Research 109: 298-309.
references: Lim KY, Kovarik A, Matyasek R, Chase MW, Knapp S, McCarthy E, Clarkson JJ, Leitch AR. 2006a. Comparative genomics and repetitive sequence divergence in the species of diploid Nicotiana section Alatae. Plant Journal 48: 907-919.
references: Lim KY, Souckova-Skalicka K, Sarasan V, Clarkson JJ, Chase MW, Kovarik A, Leitch AR. 2006b. A genetic appraisal of a new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco. American Journal of Botany 93: 875-883.
references: Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471-476.
references: Liu B, Brubaker CL, Mergeai G, Cronn RC, Wendel JF. 2001. Polyploid formation in cotton is not accompanied by rapid genomic changes. Genome 44: 321-330.
references: Ma JX, Bennetzen JL. 2006. Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proceedings of the National Academy of Sciences, USA 103: 383-388.
references: Ma JX, Devos KM, Bennetzen JL. 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Research 14: 860-869.
references: Melayah D, Lim KY, Bonnivard E, Chalhoub B, De Borne FD, Mhiri C, Leitch AR, Grandbastien MA. 2004. Distribution of the Tnt1 retrotransposon family in the amphidiploid tobacco (Nicotiana tabacum) and its wild Nicotiana relatives. Biological Journal of the Linnean Society 82: 639-649.
references: Murad L, Lim KY, Christopodulou V, Matyasek R, Lichtenstein CP, Kovarik A, Leitch AR. 2002. The origin of tobacco's T genome is traced to a particular lineage within Nicotiana tomentosiformis (Solanaceae). American Journal of Botany 89: 921-928.
references: Ozkan H, Levy AA, Feldman M. 2001. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13: 1735-1747.
references: Papp I, Iglesias VA, Moscone EA, Michalowski S, Spiker S, Park YD, Matzke MA, Matzke AJM. 1996. Structural instability of a transgene locus in tobacco is associated with aneuploidy. Plant Journal 10: 469-478.
references: Petit M. 2007. Diversité génétique et éléments transposables chez le tabac (Nicotiana tabacum): impact de l’allopolyploïdie. PhD Thesis. Paris, France: Université Paris-Sud 11 (Orsay).
references: Petit M, Lim KY, Julio E, Poncet C, Dorlhac de Borne F, Kovarik A, Leitch AR, Grandbastien MA, Mhiri C. 2007. Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (N. tabacum). Molecular Genetics and Genomics. doi: 10.1007/s00438-007-0226-0
references: Skalicka K, Lim KY, Matyasek R, Koukalova B, Leitch AR, Kovarik A. 2003. Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. American Journal of Botany 90: 988-996.
references: Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A. 2005. Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytologist 166: 291-303.
references: Soltis DE, Soltis PS, Tate JA. 2004. Advances in the study of polyploidy since plant speciation. New Phytologist 161: 173-191.
references: Song KM, Lu P, Tang KL, Osborn TC. 1995. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proceedings of the National Academy of Sciences, USA 92: 7719-7723.
references: Udall JA, Wendel JF. 2006. Polyploidy and crop improvement. Crop Science 46: S3-S14.
references: Walling JG, Shoemaker R, Young N, Mudge J, Jackson S. 2006. Chromosome-level homeology in paleopolyploid soybean (Glycine max) revealed through integration of genetic and chromosome maps. Genetics 172: 1893-1900.
references: Wells PV. 1960. Variation in section Trigonophyllae of Nicotiana. Madroño 15: 148-151.
references: Wendel JF, Schnabel A, Seelanan T. 1995. Bidirectional Interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proceedings of the National Academy of Sciences, USA 92: 280-284.
references: Zhao XP, Si Y, Hanson RE, Crane CF, Price HJ, Stelly DM, Wendel JF, Paterson AH. 1998. Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Research 8: 479-492.