Abstract
Transposable elements (TEs) dominate the genetic capacity of most eukaryotes, especially plants, where they may compose up to 90% of the genome. Many studies, both in plants and animals reported that in fact non-autonomous elements that have lost their protein-coding sequences and became miniature elements were highly associated with genes, and showed a high level of transpositional activity such as mPing family in rice. In this study, we have investigated in detail the copy number, insertional polymorphism and the methylation status of the tiniest LTR retrotransposon family, termed TRIM, in nine rice strains, in comparison with mPing. While TRIM showed similar copy numbers (average of 79 insertions) in all the nine rice strains, the copy number of mPing varied dramatically (ranging from 6 to 203 insertions) in the same strains. Site-specific PCR analysis revealed that ~58% of the TRIM elements have identical insertion sites among the nine rice strains, while none of the mPing elements (100% polymorphism) have identical insertion sites in the same strains. Finally, over 65% of the TRIM insertion sites were cytosine methylated in all nine rice strains, while the level of the methylated mPing insertion sites ranged between 43 and 81.5%. The findings of this study indicate that unlike mPing, TRIM is most probably a fossil TE family in rice. In addition, the data shows that there might be a strong correlation between TE methylation and copy number.
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References
Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143
Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368
Fukao T, Bailey-Serres J, Yeung E (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23(1):412–427
Gehring M, Henikoff S (2008) DNA methylation and demethylation in Arabidopsis. The arabidopsis book, American Society of Plant Biologists, pp 1-14
Han Y, Burnette JM 3rd, Wessler SR (2009) TARGeT: a web-based pipeline for retrieving and characterizing gene and transposable element families from genomic sequences. Nucleic Acids Res 37(11):e78
Iida S, Morita Y, Choi JD, Park KI, Hoshino A (2004) Genetics and epigenetics in flower pigmentation associated with transposable elements in morning glories. Adv Biophys 38:141–159
Jiang N, Bao ZR, Zhang XY, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421(6919):163–167
Jiang N, Feschotte C, Zhang XY, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7(2):115–119
Kashkush K, Khasdan V (2007) Large-scale survey of cytosine methylation of retrotransposons, and the impact of readout transcription from LTRs on expression of adjacent rice genes. Genetics 177:1975–1985
Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genet 33(1):102–106
Kikuchi K, Terauchi K, Wada M, Hirano HY (2003) The plant MITE mPing is mobilized in anther culture. Nature 421(6919):167–170
Kishima Y, Takata M, Kiyohara A, Takasu A, Ohtsubo H, Sano Y (2007) Rice transposable elements are characterized by various methylation environments in the genome. BMC Genomics 8:469
Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K (2010) Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186(3):801–889
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Lockton S, Gaut BS (2009) The contribution of transposable elements to expressed coding sequence in Arabidopsis thaliana. J Mol Evol 68(1):80–89
Madlung A, Comai L (2004) The effect of stress on genome regulation and structure. Ann Bot London 94(4):481–495
Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411(6834):212–214
Naito K, Cho E, Yang GJ, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103(47):17620–17625
Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461(7267):1130–1232
Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T (2003) Mobilization of a transposon in the rice genome. Nature 421(6919):170–172
Ngezahayo F, Xu CM, Wang HY, Jiang LL, Pang JS, Liu B (2009) Tissue culture-induced transpositional activity of mPing is correlated with cytosine methylation in rice. BMC Plant Biol 9:91. doi:10.1186/1471-2229-9-91
Rabinowicz PD, Palmer LE, May BP, Hemann MT, Lowe SW, McCombie WR, Martienssen RA (2003) Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res 13(12):2658–2664
Sabot F, Guyot R, Wicker T, Chantret N, Laubin B, Chalhoub B, Leroy P, Sourdille P, Bernard M (2005) Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol Genet Gen 274(2):119–130
SAS Institute Inc. (1995) JMP statistics and graphic guide
Shan X, Liu Z, Dong Z, Wang Y, Chen Y, Lin X, Long L, Han F, Dong Y, Liu B (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22(4):976–990
Singer T, Yordan C, Martienssen RA (2001) Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene decrease in DNA methylation (DDM1). Genes Dev 15(5):591–602
Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8(4):272–285
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982
Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98(24):13778–13783
Xing JC, Zhang YH, Han K, Salem AH, Sen SK, Huff CD, Zhou Q, Kirkness EF, Levy S, Batzer MA, Jorde LB (2009) Mobile elements create structural variation: analysis of a complete human genome. Genome Res 19(9):1516–1526
Xiong LZ, Xu CG, Maroof MAS, Zhang QF (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261(3):439–446
Yaakov B, Kashkush K (2011) Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54(1):42–49
Yang GJ, Nagel DH, Feschotte C, Hancock CN, Wessler SR (2009) Tuned for transposition: molecular determinants underlying the hyperactivity of a Stowaway MITE. Science 325(5946):1391–1394
Zhu Q, Ge S (2005) Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 167 (2):632-632 (vol 167, pg 249, 2005)
Zou XH, Zhang FM, Zhang JG, Zang LL, Tang L, Wang J, Sang T, Ge S (2008) Analysis of 142 genes resolves the rapid diversification of the rice genus. Genome Biol 9(3):R49
Acknowledgments
The authors would like to thank Abeer Abu-Siam for help in the lab and Beery Yaakov for helpful discussions. This work was supported by a grant from the Israel Science Foundation (Grant # 142/08) to K. K.
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Communicated by M. Jordan.
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Baruch, O., Kashkush, K. Analysis of copy-number variation, insertional polymorphism, and methylation status of the tiniest class I (TRIM) and class II (MITE) transposable element families in various rice strains. Plant Cell Rep 31, 885–893 (2012). https://doi.org/10.1007/s00299-011-1209-5
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DOI: https://doi.org/10.1007/s00299-011-1209-5