Abstract
In a previous study, we observed that the variations in chromosome size are due to uneven expansion and contraction by comparing the structures and sizes of a pair of homoeologous high-resolution cytogenetic maps of chromosomes 12A and 12D in tetraploid cotton. To reveal the variation at the sequence level, in the present paper, we sequenced two pairs of homoeologous bacterial artificial chromosomes derived from high- to low-variable genomic regions. Comparisons of their sequence variations confirmed that the highly conserved and divergent sequences existed in the distal and pericentric regions, e.g., high- and low-variable genome size regions in these two pairs of cotton homoeologous chromosomes. Sequence analysis also confirmed that the differential accumulation of Gossypium retrotransposable gypsy-like element (Gorge3) accounted for the main contributions for the size difference between the pericentric regions. By fluorescence in situ hybridization analysis, we found that Gorge3 has a bias distribution in the AT/A proximal regions and is associated with the heterochromatin along the chromosomes in the entire Gossypium genome. These results indicate that, between AT/A and DT/D genomes, the distal and pericentric regions usually possess high level of sequence conservation and divergence, respectively, in cotton.
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Bensasson D, Petrov DA, Zhang D-X, Hartl DL, Hewitt GM (2001) Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol Biol Evol 18:246–253
Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED, Sidow A, Batzoglou S (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13:721–731
Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94
Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier M-C, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701
Cronn RC, Small RL, Haselkorn T, Wendel JF (2002) Rapid diversification of the cotton genus (Gossypium: Malvaceae) revealed by analysis of sixteen nuclear and chloroplast genes. Am J Bot 89:707–725
Deutsch M, Long M (1999) Intron–exon structures of eukaryotic model organisms. Nucleic Acids Res 27:3219–3228
Dooner HK, Weil CF (2007) Give-and-take: interactions between DNA transposons and their host plant genomes. Curr Opin Genet Dev 17:486–492
Grover CE, Kim H, Wing RA, Paterson AH, Wendel JF (2004) Incongruent patterns of local and global genome size evolution in cotton. Genome Res 14:1474–1482
Grover CE, Kim H, Wing RA, Paterson AH, Wendel JF (2007) Microcolinearity and genome evolution in the AdhA region of diploid and polyploid cotton (Gossypium). Plant J 50:995–1006
Guo W, Cai C, Wang C, Zhao L, Wang L, Zhang T (2008) A preliminary analysis of genome structure and composition in Gossypium hirsutum. BMC Genomics 9:314
Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16:1252–1261
Hawkins JS, Proulx SR, Rapp RA, Wendel JF (2009) Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci USA 106:17811–17816
Hendrix B, Stewart JM (2005) Estimation of the nuclear DNA content of Gossypium species. Ann Bot 95:789–797
Hu Y, Guo WZ, Zhang TZ (2009) Construction of a bacterial artificial chromosome library of TM-1, a standard line for genetics and genomics in upland cotton. J Integr Plant Biol 51:107–112
Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467
Kapuscinski J (1995) DAPI: a DNA-specific fluorescent probe. Biotech Histochem 70:220–233
Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7:474
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33:6494–6506
Pearce S, Pich U, Harrison G, Flavell A, Heslop-Harrison J, Schubert I, Kumar A (1996) The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the terminal eterochromatin Chromosome Res 4:357–364
Peterson-Burch B, Nettleton D, Voytas D (2004) Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biol 5:R78
Petrov DA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61:531–544
Sanmiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82:37–44
SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45
Seelanan T, Schnabel A, Wendel JF (1997) Congruence and consensus in the cotton tribe (Malvaceae). Syst Bot 22:259–290
Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643
Wang K, Zhang YJ, Guan B, Guo W, Zhang T (2007) Fluorescence in situ hybridization of bacterial artificial chromosome in cotton. Prog Biochem Biophys 34:1216–1222
Wang K, Yang Z, Shu C, Hu J, Lin Q, Zhang W, Guo W, Zhang T (2009) Higher axial-resolution and sensitivity pachytene fluorescence in situ hybridization protocol in tetraploid cotton. Chromosome Res 17:1041–1050
Wang K, Guo W, Yang Z, Hu Y, Zhang W, Zhou B, Stelly D, Chen Z, Zhang T (2010) Structure and size variations between 12A and 12D homoeologous chromosomes based on high-resolution cytogenetic map in allotetraploid cotton. Chromosoma 119:255–266
Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci USA 86:4132–4136
Wendel JF, Cronn RC, Alvarez I, Liu B, Small RL, Senchina DS (2002) Intron size and genome size in plants. Mol Biol Evol 19:2346–2352
Acknowledgments
We thank Dr. Jiming Jiang and Russell J. Kohel for revisingthe manuscript, Xiaowei Niu and Yanjie Jiang for the technical assistance, and Xiangdong Chen for the analysis of Gorge3-like retrotransposons. This work was supported by the National Natural Science Foundation of China (30700510, 31071460) and New Century Excellent Talents in University (NCET-10-0496). This work was also supported partly by The Priority Academic Program Development of Jiangsu Higher Education Institutions.
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Communicated by P. Heslop-Harrison.
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Wang, K., Zhang, W., Cao, Y. et al. Localization of high level of sequence conservation and divergence regions in cotton. Theor Appl Genet 124, 1173–1182 (2012). https://doi.org/10.1007/s00122-011-1777-3
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DOI: https://doi.org/10.1007/s00122-011-1777-3