Alix, Karine, Joets, Johann, Ryder, Carol D., Moore, Jonathan D., Barker, Guy C., Bailey, John P., King , Graham J. and Heslop-Harrison, J. (John). (2008) The CACTA transposon Bot1 played a major role in Brassica genome divergence and gene proliferation. Plant Journal, Vol.56 (No.6). pp. 1030-1044. ISSN 0960-7412

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Abstract

We isolated and characterized a Brassica C genome-specific CACTA element, which was designated Bot1 (Brassica oleracea transposon 1). After analysing phylogenetic relationships, copy numbers and sequence similarity of Bot1 and Bot1 analogues in B. oleracea (C genome) versus Brassica rapa (A genome), we concluded that Bot1 has encountered several rounds of amplification in the oleracea genome only, and has played a major role in the recent rapa and oleracea genome divergence. We performed in silico analyses of the genomic organization and internal structure of Bot1, and established which segment of Bot1 is C-genome specific. Our work reports a fully characterized Brassica repetitive sequence that can distinguish the Brassica A and C chromosomes in the allotetraploid Brassica napus, by fluorescent in situ hybridization. We demonstrated that Bot1 carries a host S locus-associated SLL3 gene copy. We speculate that Bot1 was involved in the proliferation of SLL3 around the Brassica genome. The present study reinforces the assumption that transposons are a major driver of genome and gene evolution in higher plants.

Item Type:	Journal Article
Subjects:	S Agriculture > SB Plant culture Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Brassica oleracea, Brassica rapa, Genomics, Transposons
Journal or Publication Title:	Plant Journal
Publisher:	Blackwell
ISSN:	0960-7412
Date:	22 August 2008
Volume:	Vol.56
Number:	No.6
Page Range:	pp. 1030-1044
Identification Number:	10.1111/j.1365-313X.2008.03660.x
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Organisation for Economic Co-operation and Development (OECD), National Science Foundation (U.S.) (NSF)
References:	AGI, Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. /ature, 408, 796-815. Alix, K., Baurens, F.-C., Paulet, F., Glaszmann, J.-C. and D’Hont, A. (1998) Isolation and characterization of a satellite DNA family in the Saccharum complex. Genome, 41, 854-864. Alix, K. and Heslop-Harrison, J.S. (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol. Biol. 54, 895-909. Alix, K., Ryder, C.D., Moore, J., King, G.J. and Heslop-Harrison, J.S. (2005) The genomic organization of retrotransposons in Brassica oleracea. Plant Mol. Biol. 59, 839-851. Bandelt, H.-J., Forster, P. and Rohl, A. (1999) Median-Joining Networks for Inferring Intraspecific Phylogenies. Mol. Biol. Evol. 16, 37–48. Bateman, A.J. (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity, 9, 52-68. Bennetzen, J.L. (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr. Opin. Genet. Dev. 15, 621-627. Brunner, S., Pea, G. and Rafalski, A. (2005) Origins, genetic organization and transcription of a family of non-autonomous helitron elements in maize. Plant J. 43, 799-810. Casacuberta, J.M. and Santiago, N. (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene, 311, 1-11. Cui, Y., Brugière, N., Jackman, L., Bi, Y.-M. and Rothstein, S.J. (1999) Structural and transcriptional comparative analysis of the S locus regions in two selfincompatible Brassica napus lines. Plant Cell, 11, 2217-2231. Darling, A.C.E., Mau, B., Blattner, F.R. and Perna, N.T. (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394-1403. DeMarco, R., Venancio, T.M. and Verjovski-Almeida, S. (2006) SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily. BMC Evol. Biol. 6, 89. Deragon, J.-M., Landry, B.S., Pélissier, T., Tutois, S., Tourmente, S. and Picard, G. (1994) An analysis of retroposition in plants based on a family of SINEs from Brassica napus. J. Mol. Evol. 39, 378-386. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. /ucleic Acids Res. 32, 1792-1797. Eichler, E.E. and Sankoff, D. (2003) Structural dynamics of eukaryotic chromosome evolution. Science, 301, 793-797. Fedoroff, N. (2000) Transposons and genome evolution in plants. Proc. /atl. Acad. Sci. USA, 97, 7002-7007. Feschotte, C., Jiang, N. and Wessler, S.R. (2002) Plant transposable elements: where genetics meets genomics. /at. Rev. Genet. 3, 329-341. Gaeta, R.T., Pires, J.C., Iniguez-Luy, F., Leon, E. and Osborn, T.C. (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell, 19, 3403 - 3417. Gish, W.R. (2006) WU-BLAST archives: http://blast.wustl.edu/. Grandbastien, M.-A. (1998) Activation of plant transposons under stress conditions. Trends Plant Sci. 3, 181-187. Hawkins, J.S., Kim, H., Nason, J.D., Wing, R.A. and Wendel, J.F. (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 16, 1252-1261. He, Z.H., Dong, H.T., Dong, J.X., Li, D.B. and Ronald, P.C. (2000) The rice Rim2 transcript accumulates in respone to Magnaporthe grisea and its predicted protein product shares similarity with TNP2-like proteins encoded by CACTA transposons. Mol. Gen. Genet. 264, 2-10. Heslop-Harrison, J.S. (2000) Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell, 12, 617-635. IHGSC (2001) Initial sequencing and analysis of the human genome. /ature, 409, 860- 921. Inaba, R. and Nishio, T. (2002) Phylogenetic analysis of Brassicaceae based on the nucleotide sequences of the S-locus related gene, SLR1. Theor. Appl. Genet. 105, 1159-1165. Inagaki, Y., Hisatomi, Y., Suzuki, T., Kasahara, K. and Iida, S. (1994) Isolation of a Suppressor-mutator/Enhancer-like transposable element, Tpn1, from Japanese morning glories. Genes Genet. Syst. 74, 141-147. Itoh, Y., Hasebe, M., Davies, E., Tadeka, J. and Ozeki, Y. (2003) Survical of Tdc transposable elements of the En/Spm superfamily in the carrot genome. Mol. Genet. Genomics, 269, 49-59. Jacobs, G., Dechyeva, D., Menzel, G., Dombrowski, C. and Schmidt, T. (2006) Molecular characterization of Vulmar1, a complete mariner transposon of sugar beet and diversity of mariner- and En/Spm-like sequences in the genus Beta. Genome, 47, 1192–1201. Jiang, N., Bao, Z., Zhang, X., Eddy, S.R. and Wessler, S.R. (2004) Pack-MULE transposable elements mediate gene evolution in plants. /ature, 431, 569-573. Johnston, J.S., Pepper, A.E., Hall, A.E., Chen, Z.J., Hodnett, G., Drabek, J., Lopez, R. and Price, H.J. (2005) Evolution of genome size in Brassicaceae. Ann. Bot. 95, 229–235. Kapitonov, V.V. and Jurka, J. (2001) Rolling-circle transposons in eukaryotes. Proc. /atl. Acad. Sci. USA, 98, 8714-8719. Kapitonov, V.V. and Jurka, J. (2007) Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet. 23, 521-529. Kawasaki, S. and Nitasaka, E. (2004) Characterization of Tpn1 family in the Japanese morning glory: En/Spm-related transposable elements capturing host genes. Plant Cell Physiol. 45, 933-944. Kazazian, H.H. (2004) Mobile elements: drivers of genome evolution. Science, 303, 1626-1632. Kubis, S.E., Castilho, A.M.M.F., Vershinin, A.V. and Heslop-Harrison, J.S. (2003) Retroelements, transposons and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation. Plant Mol. Biol. 52, 69-79. Kuhn, G.C.S., Sene, F.M., Moreira-Filho, O., Schwarzacher, T. and Heslop-Harrison, J.S. (2008) Sequence analysis, chromosomal distribution and long-range organization show that rapid turnover of new and old pBuM satellite DNA repeats leads to different patterns of variation in seven species of the Drosophila buzzatii cluster. Chromosome Res. 16, 307-324. Kurtz, S., Choudhuri, J.V., Ohlebusch, E., Schleiermacher, C., Stoye, J. and Giegerich, R. (2001) REPuter: The manifold applications of repeat analysis on a genomic scale. /ucleic Acids Res. 29, 4633-4642. Le, Q.H., Wright, S., Yu, Z. and Bureau, T. (2000) Transposon diversity in Arabidopsis thaliana. Proc. /atl. Acad. Sci. USA, 97, 7276-7381. Leflon, M., Eber, F., Letanneur, J.-C., Chelysheva, L., Coriton, O., Huteau, V. Ryder, C.D., Barker, G., Jenczewski, E. and Chèvre, A.-M. (2006) Pairing and recombination at meiosis of Brassica rapa (AA) × Brassica napus (AACC) hybrids. Theor. Appl. Genet. 113, 1467-1480. Lenoir, A., Cournoyer, B., Warwick, S., Picard, G. and Deragon, J.-M. (1997) Evolution of SINE S1 retroposons in Cruciferae plant species. Mol. Biol. Evol. 14, 934-941. Lysak, M.A., Koch, M.A., Pecinka, A. and Schubert, I. (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res. 15, 516-525. Maddison, W.P. and Maddison, D.R. (2005) Mesquite: A modular system for evolutionary analysis. Version 1.06. http://mesquiteproject.org. Meyers, B.C., Tingey, S.V. and Morgante, M. (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11, 1660-1676. Miura, A., Yonebayashi, S., Watanabe, K., Toyama, T., Shimada, H. and Kakutani, T. (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. /ature, 411, 212-214. Morgante, M. (2006) Plant genome organisation and diversity: the year of the junk! Curr. Opin. Biotechnol. 17, 168-173. Morgante, M., Brunner, S., Pea, G., gler, K., zuccolo, A. and Rafalski, A. (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. /at. Genet. 37, 997-1002. Nacken, W.K., Piotrowiak, R., Saedler, H. and Sommer, H. (1991) The transposable element Tam1 from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol. Gen. Genet. 228, 201-208. Nicolas, S., Le Mignon, G., Eber, F., Coriton, O., Monod, H., Clouet, V., Huteau, V. Lostanlen, A., Delourme, R., Chalhoub, B., Ryder, C.D., Chèvre, A.-M. and Jenczewski, E. (2007) Homeologous recombination plays a major role in chromosome rearrangements that occur during meiosis of Brassica napus haploids. Genetics, 175, 487-503. O’Neill, C.M. and Bancroft, I. (2000) Comparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homoeologous to sequenced regions of chromosomes 4 and 5 of Arabidospis thaliana. Plant J. 23, 233-243. Ozeki, Y., Davies, E. and Takeda, J. (1997) Somatic variation during long-term subculturing of plant cells caused by insertion of a transposable element in a phenylalanine ammonia-lyase (PAL) gene. Mol. Gen. Genet. 254, 407-416. Peterson, P.A. (1953) A mutable pale green locus in maize. Genetics, 45, 115-133. Pereira, A., Cuypers, H., Gierl, A., Sommers, Z.S. and Saedler, H. (1986) Molecular analysis of the En/Spm transposable element system of Zea mays. EMBO J. 5, 835-841. Posada, D. and Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818. Rocarro, M., Li, Y., Masiero, S., Saedler, H. and Sommer, H. (2005) ROSINA (RSI), a novel protein with DNA-binding capacity, acts during floral organ development in Antirrhinum majus. Plant J. 43, 238-250. Rodríguez, F.J., Oliver, J.L., Marín, A. and Medina, J.R. (1990) The general stochastic model of nucleotide substitution. J. Theor. Biol. 142, 485-501. Schwarzacher, T. and Heslop-Harrison, J.S.(P.). (2000) Practical in situ hybridization. BIOS Scientific Publishers Ltd, Oxford, UK. Shiba, H., Takayama, S., Iwano, M., Shimosato, H., Funato, M., Nakagawa, T., Che, F.- S., Suzuki, G., Watanabe, M., Hinata, K. and Isogai, A. (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125, 2095-2103. Snowden, K.C. and Napoli, C.A. (1998) Ps1: a novel Spm-like transposable element from Petunia hybrida. Plant J. 14, 43-54. Snowdon, R.J., Köhler, W., Friedt, W. and Köhler, A. (1997) Genomic in situ hybridization in Brassica amphiploids and interspecific hybrids. Theor. Appl. Genet. 95, 1320-1324. Sonnhammer, E.L.L. and Durbin, R. (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene, 167, GC1-GC10. Strachan, T., Webb, D. and Dover, G. (1985) Transition stages of molecular drive in multiple-copy DNA families in Drosophila. EMBO J. 4, 1701-1708. Suzuki, G., Kai, N., Hirose, T., Fukui, K., Nishio, T., Takayama, S., Isogai, A., Watanabe, M. and Hinata, K. (1999) Genomic organization of the S locus: identification and charcterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics, 153, 391-400. Swofford, D.L. (2002) PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods); Version 4. Sinauer associates, Sunderland, MA. Talbert, L.E. and Chandler, V.L. (1988) Characterization of a highly conserved sequence related to mutator transposable elements in maize. Mol. Biol. Evol. 5, 519-529. Town, C.D., Cheung, F., Maiti, R., Crabtree, J., Haas, B.J., Wortman, J.R., Hine, E.E., Althoff, R., Arbogast, T.S., Tallon, L.J., Vigouroux, M., Trick, M. and Bancroft, I. (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell, 18, 1348-1359. Turcotte, K., Srinivasan, S. and Bureau, T.E. (2001) Survey of transposable elements from rice genomic sequences. Plant J. 25, 169-179. U, N. (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot. 7, 389-452. Vicient, C.M., Jääskeläinen, M.J., Kalendar, R. and Schulman, A.H. (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol. 125, 1283-1292. Walbot, V. and Petrov, D.A. (2001) Gene galaxies in the maize genome. Proc. /atl. Acad. Sci. USA, 98, 8163-8164. Wang, G.-D., Tian, P.-F., Cheng, Z.-K., Wu, G., Jiang, J.-M., Li, D.-B., Li, Q. and He, Z.-H. (2003) Genomic characterization of Rim2 / Hipa elements reveals a CACTA-like transposon superfamily with unique features in the rice genome. Mol. Gen. Genomics, 270, 234-242. Wendel, J.F. (2000) Genome evolution in polyploids. Plant Mol. Biol. 42, 225-249. Wicker, T., Guyot, R., Yahiaoui, N. and Keller, B. (2003) CACTA transposons in Triticeae. A diverse family of high-copy repetitive elements. Plant Physiol. 132, 52-63. Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., SanMiguel, P. and Schulman, A.H. (2007) A unified classification system for eukaryotic transposable elements. /at. Rev. Genet. 8, 973-982. Yang, T.-J., Kwon, S.-J., Choi, B.-S., Kim, J.S., Jin, M., Lim, K.-B., Park, J.Y., Kim, J.- A., Lim, M.-H., Kim, H.-I., Lee, H.-J., Lim, Y.P., Paterson, A.H. and Park, B.-S. (2007) Characterization of terminal-repeat retrotransposon in miniature (TRIM) in Brassica relatives. Theor. Appl. Genet. 114, 627-636. Yang, Y.W., Lai, K.N., Tai, P.Y. and Li, W.H. (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597-604. Yu, Z., Wright, S.I. and Bureau, T.E. (2000) Mutator-like elements in Arabidopsis thaliana: Structure, diversity and evolution. Genetics, 156, 2019-2031. Zabala, G. and Vodkin, L.O. (2005) The wp mutation of Glycine max carries a genefragment- rich transposon of the CACTA superfamily. Plant Cell, 17, 2619-2632. Zabala, G. and Vodkin, L. (2007) Novel exon combinations generated by alternative splicing of gene fragments mobilized by a CACTA transposon in Glycine max. BMC Plant Biol. 7, 38. Zhang, X. and Wessler, S.R. (2004) Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc. /atl. Acad. Sci. USA, 101, 5589-5594. Zhang, X. and Wessler, S.R. (2005) BoS: a large and diverse family of short interspersed elements (SINEs) in Brassica oleracea. J. Mol. Evol. 60, 677-687.
URI:	http://wrap.warwick.ac.uk/id/eprint/379

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