Abstract
Retrotransposons constitute a large portion of plant genomes. The chromosomal distribution of a wide variety of retrotransposons has been analyzed using genome sequencing data in several plants, but the evolutionary profile of transposition has been characterized for a limited number of retrotransposon families. Here, we characterized 96 elements of the SORE-1 family of soybean retrotransposons using genome sequencing data. Insertion time of each SORE-1 element into the genome was estimated on the basis of sequence differences between the 5′ and 3′ long terminal repeats (LTRs). Combining this estimation with information on the chromosomal location of these elements, we found that the insertion of the existing SORE-1 into gene-rich chromosome arms occurred on average more recently than that into gene-poor pericentromeric regions. In addition, both the number of insertions and the proportion of insertions into chromosome arms profoundly increased after 1 million years ago. Solo LTRs were detected in these regions at a similar frequency, suggesting that elimination of SORE-1 via unequal homologous recombination was unbiased. Taken together, these results suggest the preference of a recent insertion of SORE-1 into chromosome arms comprising euchromatic regions. This notion is contrary to an earlier view deduced from an overall profiling of soybean retrotransposons and suggests that the pattern of chromosomal distribution can be more diverse than previously thought between different families of retrotransposons.
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Abbreviations
- LTR:
-
Long terminal repeat
- mya:
-
Million years ago
- Wm82:
-
Williams 82
- SORE-1 :
-
SOybean RetroElement 1
- ORF:
-
Open reading frame
References
Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, Westerman RP, Sanmiguel PJ, Bennetzen JL (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732
Bushman FD (2003) Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115:135–138
Courtial B, Feuerbach F, Eberhard S, Rohmer L, Chiapello H, Camilleri C, Lucas H (2001) Tnt1 transposition events are induced by in vitro transformation of Arabidopsis thaliana, and transposed copies integrate into genes. Mol Gen Genomics 265:32–42
Dai J, Xie W, Brady TL, Gao J, Voytas DF (2007) Phosphorylation regulates integration of the yeast Ty5 retrotransposon into heterochromatin. Mol Cell 27:289–299
Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079
Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, Shoemaker RC, Ma J (2010a) Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J 63:584–598
Du J, Grant D, Tian Z, Nelson RT, Zhu L, Shoemaker RC, Ma J (2010b) SoyTEdb: a comprehensive database of transposable elements in the soybean genome. BMC Genomics 11:113
Fukai E, Soyano T, Umehara Y, Nakayama S, Hirakawa H, Tabata S, Sato S, Hayashi M (2012) Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J 69:720–730
Gao X, Hou Y, Ebina H, Levin HL, Voytas DF (2008) Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res 18:359–369
Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843–D846
Hou Y, Rajagopal J, Irwin PA, Voytas DF (2010) Retrotransposon vectors for gene delivery in plants. Mob DNA 1:19
International Rice Genome Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Kanazawa A, Liu B, Kong F, Arase S, Abe J (2009) Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J Mol Evol 69:164–175
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Le QH, Melayah D, Bonnivard E, Petit M, Grandbastien MA (2007) Distribution dynamics of the Tnt1 retrotransposon in tobacco. Mol Gen Genomics 278:639–651
Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180:995–1007
Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410
Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869
Masuta Y, Nozawa K, Takagi H, Yaegashi H, Tanaka K, Ito T, Saito H, Kobayashi H, Matsunaga W, Masuda S, Kato A, Ito H (2017) Inducible transposition of a heat-activated retrotransposon in tissue culture. Plant Cell Physiol 58:375–384
Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, Cao J, Weigel D, Paszkowski J, Mathieu O (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430
Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780
Okamoto H, Hirochika H (2000) Efficient insertion mutagenesis of Arabidopsis by tissue culture-induced activation of the tobacco retrotransposon Tto1. Plant J 23:291–304
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5:R79
Peterson-Burch BD, Voytas DF (2002) Genes of the Pseudoviridae (Ty1/copia retrotransposons). Mol Biol Evol 19(11):1832–1845
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tian Z, Rizzon C, Du J, Zhu L, Bennetzen JL, Jackson SA, Gaut BS, Ma J (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res 19:2221–2230
Tian Z, Zhao M, She M, Du J, Cannon SB, Liu X, Xu X, Qi X, Li MW, Lam HM, Ma J (2012) Genome-wide characterization of nonreference transposons reveals evolutionary propensities of transposons in soybean. Plant Cell 24:4422–4436
Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–426
Tsukahara S, Kawabe A, Kobayashi A, Ito T, Aizu T, Shin-i T, Toyoda A, Fujiyama A, Tarutani Y, Kakutani T (2012) Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev 26:705–713
Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20:528–540
Xu Y, Du J (2014) Young but not relatively old retrotransposons are preferentially located in gene-rich euchromatic regions in tomato (Solanum lycopersicum) plants. Plant J 80:582–591
Zhao C, Takeshima R, Zhu J, Xu M, Sato M, Watanabe S, Kanazawa A, Liu B, Kong F, Yamada T, Abe J (2016) A recessive allele for delayed flowering at the soybean maturity locus E9 is a leaky allele of FT2a, a FLOWERING LOCUS T ortholog. BMC Plant Biol 16:20
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This work is supported in part by JSPS KAKENHI Grant Number JP17H03743.
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Nakashima, K., Abe, J. & Kanazawa, A. Chromosomal distribution of soybean retrotransposon SORE-1 suggests its recent preferential insertion into euchromatic regions. Chromosome Res 26, 199–210 (2018). https://doi.org/10.1007/s10577-018-9579-y
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DOI: https://doi.org/10.1007/s10577-018-9579-y