Co-evolution of plant LTR-retrotransposons and their host genomes

Abstract

zTransposable elements (TEs), particularly, long terminal repeat retrotransposons (LTR-RTs), are the most abundant DNA components in all plant species that have been investigated, and are largely responsible for plant genome size variation. Although plant genomes have experienced periodic proliferation and/or recent burst of LTRretrotransposons, the majority of LTR-RTs are inactivated by DNA methylation and small RNA-mediated silencing mechanisms, and/or were deleted/truncated by unequal homologous recombination and illegitimate recombination, as suppression mechanisms that counteract genome expansion caused by LTR-RT amplification. LTR-RT DNA is generally enriched in pericentromeric regions of the host genomes, which appears to be the outcomes of preferential insertions of LTR-RTs in these regions and low effectiveness of selection that purges LTR-RT DNA from these regions relative to chromosomal arms. Potential functions of various TEs in their host genomes remain blurry; nevertheless, LTR-RTs have been recognized to play important roles in maintaining chromatin structures and centromere functions and regulation of gene expressions in their host genomes.

Keywords

LTR-retrotransposons / recombination / evolution / epigenetic regulation / plants

References

[1] Aufsatz, W., Mette, M.F., van der Winden, J., Matzke, A.J.M., and Matzke, M. (2002). RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci U S A 99, 16499-16506 .10.1073/pnas.162371499
[2] Bejerano, G., Lowe, C.B., Ahituv, N., King, B., Siepel, A., Salama, S.R., Rubin, E.M., Kent, W.J., and Haussler, D. (2006). A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441, 87-90 .10.1038/nature04696
[3] Bennetzen, J.L., Ma, J., and Devos, K. (2005). Mechanisms of recent genome size variation in flowering plants. Ann Bot 95, 127-132 .10.1093/aob/mci008
[4] Cao, X., and Jacobsen, S.E. (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12, 1138-1144 .10.1016/S0960-9822(02)00925-9
[5] Chaw, S.M., Chang, C.C., Chen, H.L., and Li, W.H. (2004). Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58, 424-441 .10.1007/s00239-003-2564-9
[6] Cheng, C., Daigen, M., and Hirochika, H. (2006). Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics 276, 378-390 .10.1007/s00438-006-0141-9
[7] Cheng, Z., Dong, F., Langdon, T., Ouyang, S., Buell, C.R., Gu, M., Blattner, F.R., and Jiang, J. (2002). Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14, 1691-1704 .10.1105/tpc.003079
[8] Devos, K.M., Brown, J.K.M., and Bennetzen, J.L. (2002). Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12, 1075-1079 .10.1101/gr.132102
[9] Doolittle, W.F., and Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601-603 .10.1038/284601a0
[10] Dooner, H.K., and He, L. (2008). Maize genome structure variation: interplay between retrotransposon polymorphisms and genic recombination. Plant Cell 20, 249-258 .10.1105/tpc.107.057596
[11] Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E., and Ecker, J.R. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109, E2183-2191 .10.1073/pnas.1209329109
[12] Du, C., Swigonova, Z., and Messing, J. (2006). Retrotranspositions in orthologous regions of closely related grass species. BMC Evol Biol 6, 62.10.1186/1471-2148-6-62
[13] Du, J., Tian, Z., Hans, C.S., Laten, H.M., Cannon, S.B., Jackson, S.A., Shoemaker, R.C., and 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 .10.1111/j.1365-313X.2010.04263.x
[14] Du, J., Tian, Z., Bowen, N.J., Schmutz, J., Shoemaker, R.C., and Ma, J. (2010b). Bifurcation and enhancement of autonomous-nonautonomous retrotransposon partnership through LTR swapping in soybean. Plant Cell 22, 48-61 .10.1105/tpc.109.068775
[15] Du, J., Tian, Z., Sui, Y., Zhao, M., Song, Q., Cannon, S.B., Cregan, P.,and Ma, J. (2012). Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. Plant Cell 24, 21-32 .10.1105/tpc.111.092759
[16] Finnegan, D. J. (1989). Eukaryotic transposable elements and genome evolution. Trends Genet 5, 103-107 .10.1016/0168-9525(89)90039-5
[17] Gao, D., Chen, J., Chen, M., Meyers, B.C., and Jackson, S. (2012). A highly conserved, small LTR retrotransposon that preferentially targets genes in grass genomes. PLoS One 7, e32010.10.1371/journal.pone.0032010
[18] Gaut, B.S., Wright, S.I., Rizzon, C., Dvorak, J., and Anderson, L.K. (2007). Opinion- Recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev Genet 8, 77-84 .10.1038/nrg1970
[19] Grandbastien, M.A. (1992). Retroelements in higher-plants. Trends Genet 8, 103-108 .
[20] Hamilton, A., Voinnet, O., Chappell, L., and Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. EMBO J 21, 4671-4679 .10.1093/emboj/cdf464
[21] Hanada, K., Vallejo, V., Nobuta, K., Slotkin, R.K., Lisch, D., Meyers, B.C., Shiu, S.H., and Jiang, N. (2009). The functional role of Pack- MULEs in rice inferred from purifying selection and expression pro- file. Plant Cell 21, 25-38 .10.1105/tpc.108.063206
[22] Hashida, S., Kitamura, K., Mikami, T., and Kishima, Y. (2003). Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol 132, 1207-1216 .10.1104/pp.102.017533
[23] Hawkins, J.S., Proulx, S.R., Rapp, R.A., and Wendel, J.F. (2009). Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci U S A 106, 17811-17816 .10.1073/pnas.0904339106
[24] Hirochika, H. (1993). Activation of tobacco retrotransposons during tissue-culture. EMBO J 12, 2521-2528 .
[25] Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., and Kanda, M. (1996). Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A 93, 7783-7788 .10.1073/pnas.93.15.7783
[26] Hirochika, H., Okamoto, H., and Kakutani, T. (2000). Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357-368 .
[27] Hirochika, H. (2001). Contribution of the Tos17 retrotransposon to rice functional genomics. Curr Opin Plant Biol 4, 118-122 .10.1016/S1369-5266(00)00146-1
[28] Hollister, J.D., and Gaut, B.S. (2009). Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19, 1419-1428 .10.1101/gr.091678.109
[29] Huettel, B., Kanno, T., Daxinger, L., Bucher, E., van der Winden, J., Matzke, A.J., and Matzke, M. (2007). RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim Biophys Acta 1769, 358-374 .10.1016/j.bbaexp.2007.03.001
[30] International Rice Genome Sequencing Project. (2005). The mapbased sequence of the rice genome. Nature 436, 793-800 .10.1038/nature03895
[31] Jiang, N., Bao, Z., Temnykh, S., Cheng, Z., Jiang, J., Wing, R.A., McCouch, S.R., and Wessler, S.R. (2002a). Dasheng: A recently amplified nonautonomous long terminal repeat element that is a major component of pericentromeric regions in rice. Genetics 161, 1293-1305 .
[32] Jiang, N., Jordan, I.K., and Wessler, S.R. (2002b). Dasheng and RIRE2. A nonautonomous long terminal repeat element and its putative autonomous partner in the rice genome. Plant Physiol 130, 1697-1705 .10.1104/pp.015412
[33] Jiang, N., Bao, Z., Zhang, X., Eddy, S.R., and Wessler, S.R. (2004). Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569-573 .10.1038/nature02953
[34] Jin, Y.K., and Bennetzen, J.L. (1994). lntegration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bsl retroelement of maize. Plant Cell 6, 1177-1186 .
[35] Kalendar, R., Vicient, C.M., Peleg, O., Anamthawat-Jonsson, K., Bolshoy, A., and Schulman, A.H. (2004). Large retrotransposon derivatives: Abundant, conserved but nonautonomous retroelements of barley and related genomes. Genetics 166, 1437-1450 .10.1534/genetics.166.3.1437
[36] Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R., Jeddeloh, J.A., Riddle, N.C., Verbsky, M.L., and Richards, E.J. (2003). Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109-1122 .
[37] Kashkush, K., Feldman, M., and Levy, A.A. (2002). Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160, 1651-1659 .
[38] Kashkush, K., Feldman, M., and Levy, A.A. (2003). Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33, 102-106 .10.1038/ng1063
[39] Kashkush, K., and Khasdan, V. (2007). Large-scale survey of cytosine methylation of retrotransposons and the impact of readout transcription from long terminal repeats on expression of adjacent rice genes. Genetics 177, 1975-1985 .10.1534/genetics.107.080234
[40] Kasschau, K.D., Fahlgren, N., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., and Carrington, J.C. (2007). Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5, 479-493 .10.1371/journal.pbio.0050057
[41] 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 .10.1093/pcp/pch109
[42] Kejnovsky, E., Kubat, Z., Macas, J., Hobza, R., Mracek, J., and Vyskot, B. (2006). Retand: a novel family of gypsy-like retrotransposons harboring an amplified tandem repeat. Mol Genet Genomics 276, 254-263 .10.1007/s00438-006-0140-x
[43] Kinoshita, T., Miura, A., Choi, Y.H., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L., and Kakutani, T. (2004). One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521-523 .10.1126/science.1089835
[44] Kinoshita, Y., Saze, H., Kinoshita, T., Miura, A., Soppe, W.J.J., Koornneef, M., and Kakutani, T. (2007). Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49, 38-45 .10.1111/j.1365-313X.2006.02936.x
[45] Kraitshtein, Z., Yaakov, B., Khasdan, V., and Kashkush, K. (2010). Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186, 801-812 .10.1534/genetics.110.120790
[46] Kumar, A., and Bennetzen, J.L. (1999). Plant retrotransposons. Annu Rev Genet 33, 479-532 .10.1146/annurev.genet.33.1.479
[47] Laten, H.M., Majumdar, A., and Gaucher, E.A. (1998). SIRE-1, a copia/ Ty1-like retroelement from soybean, encodes a retroviral envelopelike protein. Proc Natl Acad Sci U S A 95, 6897-6902 .10.1073/pnas.95.12.6897
[48] Laten, H.M., Havecker, E.R., Farmer, L.M. and Voytas, D.F. (2003) SIRE1, an endogenous retrovirus family from Glycine max, is highly homogeneous and evolutionarily young. Mol Biol Evol 20, 1222-1230 .10.1093/molbev/msg142
[49] Lippman, Z., and Martienssen, R. (2004). The role of RNA interference in heterochromatic silencing. Nature 431, 364-370 .10.1038/nature02875
[50] Lisch, D. (2009). Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60, 43-66 .10.1146/annurev.arplant.59.032607.092744
[51] Lisch, D., and Bennetzen, J.L. (2011). Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 14, 156-161 .10.1016/j.pbi.2011.01.003
[52] Lu, C., Tej, S.S., Luo, S., Haudenschild, C.D., Meyers, B.C., and Green, P.J. (2005). Elucidation of the small RNA component of the transcriptome. Science 309, 1567-1569 .10.1126/science.1114112
[53] Ma, J., Devos, K.M., and Bennetzen, J.L. (2004). Analyses of LTRretrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14, 860-869 .10.1101/gr.1466204
[54] Marillonnet, S., and Wessler, S.R. (1997). Retrotransposon insertion into the maize waxy gene results in tissue-specific RNA processing. Plant Cell 9, 967-978 .10.1105/tpc.9.6.967
[55] Matzke, M.A., Kanno, T., Huettel, B., Daxinger, L., and Matzke, A.J.M.(2007). Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10, 512-519 .10.1016/j.pbi.2007.06.007
[56] Meyers, B.C., Tingey, S.V., and Morgante, M. (2001). Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 10, 1660-1676 .10.1101/gr.188201
[57] 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. Nature 411, 212-214 .10.1038/35075612
[58] Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K., and Hirochika, H. (2003). Target site speci-ficity 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 .10.1105/tpc.012559
[59] Nagaki, K., Cheng, Z., Ouyang, S., Talbert, P.B., Kim, M., Jones, K.M., Henikoff, S., Buell, C.R., and Jiang, J. (2004). Sequencing of a rice centromere uncovers active genes. Nat Genet 36, 138-145 .10.1038/ng1289
[60] Naito, K., Zhang, F., Tsukiyama, T., Saito, H., Hancock, C.N., Richardson, A.O., Okumoto, Y., Tanisaka, T., and Wessler, S.R. (2009). Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461, 1130-1134 .10.1038/nature08479
[61] Nobuta, K., Venu, R.C., Lu, C., Belo, A., Vemaraju, K., Kulkarni, K., Wang, W., Pillay, M., Green, P.J., Wang, G.L., . (2007). An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25, 473-477 .10.1038/nbt1291
[62] Nosaka, M., Itoh, J., Nagato, Y., Ono, A., Ishiwata, A., and Sato, Y. (2012). Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet 8, e1002953.10.1371/journal.pgen.1002953
[63] Ohtsubo, H., Kumekawa, N., and Ohtsubo, E. (1999). RIRE2, a novel gypsy-type retrotransposon from rice. Genes Genet Syst 74, 83-91 .10.1266/ggs.74.83
[64] Orgel, L.E., and Crick, F.H.C. (1980). Selfish DNA: the ultimate parasite. Nature 284, 604-607 .10.1038/284604a0
[65] Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., . (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556 .10.1038/nature07723
[66] Perez-Hormaeche, J., Potet, F., Beauclair, L., Le Masson, I., Courtial, B., Bouche, N., and Lucas, H. (2008). Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing. Plant Physiol 147, 1264-1278 .10.1104/pp.108.117846
[67] Piegu, B., Guyot, R., Picault, N., Roulin, A., Saniyal, A., Kim, H., Collura, K., Brar, D.S., Jackson, S., Wing, R.A., . (2006). Doubling genome size without polyploidization: Dynamics of retrotransposition- driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16, 1262-1269 .10.1101/gr.5290206
[68] Rizzon, C., Marais, G., Gouy, M., and Biemont, C. (2002). Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12, 400-407 .
[69] Sabot, F., and Schulman, A.H. (2007). Template switching can create complex LTR retrotransposon insertions in Triticeae genomes. BMC Genomics 8, 247.10.1186/1471-2164-8-247
[70] SanMiguel, P., Tikhonov, A., Jin, Y.K., Motchoulskaia, N., Zakharov, D., MelakeBerhan, A., Springer, P.S., Edwards, K.J., Lee, M., Avramova, Z., . (1996). Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765-768 .10.1126/science.274.5288.765
[71] SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y., and Bennetzen, J.L. (1998). The paleontology of intergene retrotransposons of maize. Nat Genet 20, 43-45 .10.1038/1695
[72] Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., . (2010). Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183 .10.1038/nature08670
[73] Schnable, P.S., Ware, D., Fulton, R.S., Stein, J.C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T.A., . (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115 .10.1126/science.1178534
[74] Slotkin, R.K., Freeling, M., and Lisch, D. (2005). Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37, 641-644 .10.1038/ng1576
[75] Song, S.U., Gerasimova, T., Kurkulos, M., Boeke, J.D., and Corces, V.G. (1994). An Env-like protein encoded by Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Gene Dev 8, 2026-2057 .10.1101/gad.8.17.2046
[76] Soppe, W.J.J., Jacobsen, S.E., Alonso-Blanco, C., Jackson, J.P., Kakutani, T., Koornneef, M., and Peeters, A.J.M. (2000). The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6, 791-802 .10.1016/S1097-2765(05)00090-0
[77] Steinbauerova, V., Neumann, P., Novak, P., and Macas, J. (2011). A widespread occurrence of extra open reading frames in plant Ty3/ gypsy retrotransposons. Genetica 139, 1543-1555 .10.1007/s10709-012-9654-9
[78] Sugimoto, K., Takeda, S., and Hirochika, H. (2000). MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell 12, 2511-2527 .
[79] Tadege, M., Wen, J., He, J., Tu, H., Kwak, Y., Eschstruth, A., Cayrel, A., Gabriella, E., Zhao, P.X., Chabaud, M.. (2008). Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54, 335-347 .10.1111/j.1365-313X.2008.03418.x
[80] Takeda, S., Sugimoto, K., Otsuki, H., and Hirochika, H. (1999). A 13- bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18, 383-393 .10.1046/j.1365-313X.1999.00460.x
[81] The Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815 .10.1038/35048692
[82] The International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763-768 .10.1038/nature08747
[83] Tian, Z., Rizzon, C., Du, J., Zhu, L., Bennetzen, J.L., Jackson, S.A., Gaut, B.S., and 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 .10.1101/gr.083899.108
[84] Tian, Z., Zhao, M., She, M., Du, J., Cannon, S.B., Liu, X., Xu, X., Qi, X., Li, M.W., Lam, H.M., . (2012). Genome-wide characterization of nonreference transposons reveals evolutionary propensities of transposons in soybean. Plant Cell 24, 4422-4436 .10.1105/tpc.112.103630
[85] Varagona, M.J., Purugganan, M., and Wessler, S.R. (1992). Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4, 811-820 .
[86] Vitte, C., and Bennetzen, J.L. (2006). Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci U S A 103, 17638-17643 .10.1073/pnas.0605618103
[87] Vongs, A., Kakutani, T., Martienssen, R.A., and Richards, E.J. (1993). Arabidopsis thaliana DNA methylation mutants. Science 260, 1926-1928 .10.1126/science.8316832
[88] Wang, H., and Liu, J.S. (2008). LTR retrotransposon landscape in Medicago truncatula: more rapid removal than in rice. BMC Genomics 9, 382.10.1186/1471-2164-9-382
[89] Wang, Q., and Dooner, H.K. (2006). Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci U S A 103, 17644-17649 .10.1073/pnas.0603080103
[90] Wang, W., Zheng, H., Fan, C., Li, J., Shi, J., Cai, Z., Zhang, G., Liu, D., Zhang, J., Vang, S., . (2006). High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell 18, 1791-1802 .10.1105/tpc.106.041905
[91] White, S.E., Habera, L.F., and Wessler, S.R. (1994). Retrotransposons in the flanking regions of normal plant genes- a role for copia-Like elements in the evolution of gene structure and expression. Proc Natl Acad Sci U S A 91, 11792-11796 .10.1073/pnas.91.25.11792
[92] Wicker, T., and Keller, B. (2007). Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17, 1072-1081 .10.1101/gr.6214107
[93] Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., . (2007). Aunified classification system for eukaryotic transposable elements. Nat Rev Genet 8, 973-982 .10.1038/nrg2165
[94] Wilhelm, M., and Wilhelm, F.X. (2001). Reverse transcription of retroviruses and LTR retrotransposons. Cell Mol Life Sci 58, 1246-1262 .10.1007/PL00000937
[95] Witte, C.P., Le, Q.H., Bureau, T., and Kumar, A. (2001). Terminalrepeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci U S A 98, 13778-13783 .10.1073/pnas.241341898
[96] Wright, D.A., and Voytas, D.F. (1998). Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149, 703-715 .
[97] Wright, D.A., and Voytas, D.F. (2002). Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12, 122-131 .10.1101/gr.196001
[98] 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., . (2007). Characterization of terminal-repeat retrotransposon in miniature (TRIM) in Brassica relatives. Theor Appl Genet 114, 627-636 .10.1007/s00122-006-0463-3
[99] Zhong, C.X., Marshall, J.B., Topp, C., Mroczek, R., Kato, A., Nagaki, K., Birchler, J.A., Jiang, J., and Dawe, R.K. (2002). Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14, 2825-2836 .10.1105/tpc.006106
[100] Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and Henikoff, S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39, 61-69 .10.1038/ng1929