SCIENCE CHINA Life Sciences, Volume 59 , Issue 1 : 24-37(2016) https://doi.org/10.1007/s11427-015-4993-2

The effect of transposable elements on phenotypic variation: insights from plants to humans

More info
  • ReceivedNov 12, 2015
  • AcceptedDec 16, 2015
  • PublishedJan 8, 2016


Transposable elements (TEs), originally discovered in maize as controlling elements, are the main components of most eukaryotic genomes. TEs have been regarded as deleterious genomic parasites due to their ability to undergo massive amplification. However, TEs can regulate gene expression and alter phenotypes. Also, emerging findings demonstrate that TEs can establish and rewire gene regulatory networks by genetic and epigenetic mechanisms. In this review, we summarize the key roles of TEs in fine-tuning the regulation of gene expression leading to phenotypic plasticity in plants and humans, and the implications for adaption and natural selection.

Funded by

National Natural Science Foundation of China(31210103901,31123007)

National Basic Research Program of China(2013CB835200)

State Key Laboratory of Plant Genomics(2015B0129-01)


Acknowledgements This work was supported by the National Natural Science Foundation of China (31210103901, 31123007), the National Basic Research Program of China (2013CB835200), and the State Key Laboratory of Plant Genomics (2015B0129-01). Liya Wei was supported by the China Postdoctoral Science Foundation (2015M570170).

Interest statement

Compliance and ethics The author(s) declare that they have no conflict of interest.


[1] Adam H., Jouannic S., Orieux Y., Morcillo F., Richaud F., Duval Y., Tregear J.W.. Functional characterization of MADS box genes involved in the determination of oil palm flower structure. J Exp Bot, 2007, 58: 1245-1259 CrossRef PubMed Google Scholar

[2] Barkan A., Miles D., Taylor W.C.. Chloroplast gene expression in nuclear, photosynthetic mutants of maize.. EMBO J, 1986, 5: 1421-1427 CrossRef Google Scholar

[3] Beló A., Nobuta K., Venu R.C., Janardhanan P.E., Wang G., Meyers B.C.. Transposable element regulation in rice and Arabidopsis: diverse patterns of active expression and siRNA-mediated silencing. Tropical Plant Biol, 2008, 1: 72-84 CrossRef Google Scholar

[4] Bhattacharyya M.K., Smith A.M., Ellis T.H.N., Hedley C., Martin C.. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell, 1990, 60: 115-122 CrossRef Google Scholar

[5] Boss P.K., Sreekantan L., Thomas M.R.. A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct Plant Biol, 2006, 33: 31-41 CrossRef Google Scholar

[6] Bradley D., Ratcliffe O., Vincent C., Carpenter R., Coen E.. Inflorescence commitment and architecture in Arabidopsis. Science, 1997, 275: 80-83 CrossRef PubMed Google Scholar

[7] Bundock P., Hooykaas P.. An Arabidopsis hAT-like transposase is essential for plant development. Nature, 2005, 436: 282-284 CrossRef PubMed ADS Google Scholar

[8] Butelli E., Licciardello C., Zhang Y., Liu J., Mackay S., Bailey P., Reforgiato-Recupero G., Martin C.. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 2012, 24: 1242-1255 CrossRef PubMed Google Scholar

[9] Chen S.M., Coe Jr. E.H.. Control of anthocyanin synthesis by the C locus in maize. Biochem Genet, 1977, 15: 333-346 CrossRef Google Scholar

[10] Cheng Z., Buell C.R., Wing R.A., Gu M., Jiang J.. Toward a cytological characterization of the rice genome. Genome Res, 2001, 11: 2133-2141 CrossRef PubMed Google Scholar

[11] Chiu L.W., Zhou X., Burke S., Wu X., Prior R.L., Li L.. The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiol, 2010, 154: 1470-1480 CrossRef PubMed Google Scholar

[12] Chopra S., Brendel V., Zhang J., Axtell J.D., Peterson T.. Molecular characterization of a mutable pigmentation phenotype and isolation of the first active transposable element from Sorghum bicolor. Proc Natl Acad Sci USA, 1999, 96: 15330-15335 CrossRef PubMed ADS Google Scholar

[13] Clegg M.T., Durbin M.L.. Flower color variation: a model for the experimental study of evolution. Proc Natl Acad Sci USA, 2000, 97: 7016-7023 CrossRef PubMed ADS Google Scholar

[14] Clegg M.T., Durbin M.L.. Tracing floral adaptations from ecology to molecules. Nat Rev Genet, 2003, 4: 206-215 CrossRef PubMed Google Scholar

[15] Coen E.S., Carpenter R., Martin C.. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell, 1986, 47: 285-296 CrossRef Google Scholar

[16] Cordaux R., Batzer M.A.. The impact of retrotransposons on human genome evolution. Nat Rev Genet, 2009, 10: 691-703 CrossRef PubMed Google Scholar

[17] Cowan R.K., Hoen D.R., Schoen D.J., Bureau T.E.. MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol, 2005, 22: 2084-2089 CrossRef PubMed Google Scholar

[18] Cubas P., Lauter N., Doebley J., Coen E.. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J, 1999, 18: 215-222 CrossRef Google Scholar

[19] Cui X., Cao X.. Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol, 2014, 21: 83-88 CrossRef PubMed Google Scholar

[20] Cui X., Jin P., Cui X., Gu L., Lu Z., Xue Y., Wei L., Qi J., Song X., Luo M., et al. Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci USA, 2013, 110: 1953-1958 CrossRef PubMed ADS Google Scholar

[21] Ding Y., Wang X., Su L., Zhai J.X., Cao S.Y., Zhang D.F., Liu C.Y., Bi Y.P., Qian Q., Cheng Z.K., et al. SDG714, a Histone H3K9 Methyltransferase, Is Involved in Tos17 DNA Methylation and Transposition in Rice. Plant Cell, 2007, 19: 9-22 CrossRef PubMed Google Scholar

[22] Doebley, J., Stec, A., and Gustus, C. (1995). Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141, 333–346. Google Scholar

[23] Erwin J.A., Marchetto M.C., Gage F.H.. Mobile DNA elements in the generation of diversity and complexity in the brain. Nat Rev Neurosci, 2014, 15: 497-506 CrossRef PubMed Google Scholar

[24] Fernandez L., Torregrosa L., Segura V., Bouquet A., Martinez-Zapater J.M.. Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J, 2010, 61: 545-557 CrossRef PubMed Google Scholar

[25] Feschotte C.. Transposable elements and the evolution of regulatory networks. Nat Rev Genet, 2008, 9: 397-405 CrossRef PubMed Google Scholar

[26] Feschotte C., Jiang N., Wessler S.R.. Plant transposable elements: where genetics meets genomics. Nat Rev Genet, 2002, 3: 329-341 CrossRef PubMed Google Scholar

[27] Fransz P., Armstrong S., Alonso‐blanco C., Fischer T.C., Torres‐ruiz R.A., Jones G.. Cytogenetics for the model system Arabidopsis thaliana. Plant J, 1998, 13: 867-876 CrossRef Google Scholar

[28] Fujimoto R., Kinoshita Y., Kawabe A., Kinoshita T., Takashima K., Nordborg M., Nasrallah M.E., Shimizu K.K., Kudoh H., Kakutani T., et al. Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet, 2008, 4: e1000048 CrossRef PubMed Google Scholar

[29] Gazzani S., Gendall A.R., Lister C., Dean C.. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol, 2003, 132: 1107-1114 CrossRef PubMed Google Scholar

[30] Hancks D.C., Kazazian Jr. H.H.. Active human retrotransposons: variation and disease. Curr Opin Genets Dev, 2012, 22: 191-203 CrossRef PubMed Google Scholar

[31] Hayashi K., Yoshida H.. Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J, 2009, 57: 413-425 CrossRef PubMed Google Scholar

[32] Hiltbrunner A., Tscheuschler A., Viczián A., Kunkel T., Kircher S., Schäfer E.. FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant Cell Physiol, 2006, 47: 1023-1034 CrossRef PubMed Google Scholar

[33] Hiltbrunner A., Viczián A., Bury E., Tscheuschler A., Kircher S., Tóth R., Honsberger A., Nagy F., Fankhauser C., Schäfer E.. Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr Biol, 2005, 15: 2125-2130 CrossRef PubMed Google Scholar

[34] Hong L., Qian Q., Tang D., Wang K., Li M., Cheng Z.. A mutation in the rice chalcone isomerase gene causes the golden hull and internode 1 phenotype. Planta, 2012, 236: 141-151 CrossRef PubMed Google Scholar

[35] Hori Y., Fujimoto R., Sato Y., Nishio T.. A novel wx mutation caused by insertion of a retrotransposon-like sequence in a glutinous cultivar of rice (Oryza sativa). Theor Appl Genet, 2007, 115: 217-224 CrossRef PubMed Google Scholar

[36] Huang C.R.L., Burns K.H., Boeke J.D.. Active transposition in genomes. Annu Rev Genet, 2012, 46: 651-675 CrossRef PubMed Google Scholar

[37] Javidfar F., Cheng B.. Single locus, multiallelic inheritance of erucic acid content and linkage mapping of gene in yellow mustard. Crop Sci, 2013, 53: 825-832 CrossRef Google Scholar

[38] Jeong J.S., Kim Y.S., Baek K.H., Jung H., Ha S.H., Do Choi Y., Kim M., Reuzeau C., Kim J.K.. Root-Specific Expression of OsNAC10 Improves Drought Tolerance and Grain Yield in Rice under Field Drought Conditions. Plant Physiol, 2010, 153: 185-197 CrossRef PubMed Google Scholar

[39] Jiang N., Bao Z., Zhang X., Hirochika H., Eddy S.R., McCouch S.R., Wessler S.R.. An active DNA transposon family in rice. Nature, 2003, 421: 163-167 CrossRef PubMed ADS Google Scholar

[40] Jiang N., Feschotte C., Zhang X., Wessler S.R.. Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol, 2004, 7: 115-119 CrossRef PubMed Google Scholar

[41] Joly-Lopez Z., Forczek E., Hoen D.R., Juretic N., Bureau T.E., Bennetzen J.L.. A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet, 2012, 8: e1002931 CrossRef PubMed Google Scholar

[42] Kaer K., Speek M.. Retroelements in human disease. Gene, 2013, 518: 231-241 CrossRef PubMed Google Scholar

[43] Kanazawa A., Liu B., Kong F., Arase S., Abe J.. Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J Mol Evol, 2009, 69: 164-175 CrossRef PubMed ADS Google Scholar

[44] Kawase M., Fukunaga K., Kato K.. Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol Genet Genomics, 2005, 274: 131-140 CrossRef PubMed Google Scholar

[45] Kazazian H.H., Wong C., Youssoufian H., Scott A.F., Phillips D.G., Antonarakis S.E.. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature, 1988, 332: 164-166 CrossRef PubMed ADS Google Scholar

[46] Kikuchi K., Terauchi K., Wada M., Hirano H.Y.. The plant MITE mPing is mobilized in anther culture. Nature, 2003, 421: 167-170 CrossRef PubMed ADS Google Scholar

[47] Kinoshita Y., Saze H., Kinoshita T., Miura A., Soppe W.J.J., Koornneef M., Kakutani T.. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J, 2007, 49: 38-45 CrossRef PubMed Google Scholar

[48] Kiyosawa, S. (1972). The inheritance of blast resistance transferred from some indica varieties in rice. Bull Nat Inst Agric Sci 23, 69–96. Google Scholar

[49] Kobayashi S., Goto-Yamamoto N., Hirochika H.. Retrotransposon-induced mutations in grape skin color. Science, 2004, 304: 982 CrossRef PubMed Google Scholar

[50] Kunarso G., Chia N.Y., Jeyakani J., Hwang C., Lu X., Chan Y.S., Ng H.H., Bourque G.. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet, 2010, 42: 631-634 CrossRef PubMed Google Scholar

[51] Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature, 2001, 409: 860-921 CrossRef PubMed Google Scholar

[52] Levin H.L., Moran J.V.. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet, 2011, 12: 615-627 CrossRef PubMed Google Scholar

[53] Li F., Fan G., Lu C., Xiao G., Zou C., Kohel R.J., Ma Z., Shang H., Ma X., Wu J., et al. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol, 2015, 33: 524-530 CrossRef PubMed Google Scholar

[54] Li F., Fan G., Wang K., Sun F., Yuan Y., Song G., Li Q., Ma Z., Lu C., Zou C., et al. Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet, 2014a, 46: 567-572 CrossRef PubMed Google Scholar

[55] Li Q., Xiao G., Zhu Y.X.. Single-nucleotide resolution mapping of the Gossypium raimondii transcriptome reveals a new mechanism for alternative splicing of introns. Mol Plant, 2014b, 7: 829-840 CrossRef PubMed Google Scholar

[56] Li X., Chen L., Hong M., Zhang Y., Zu F., Wen J., Yi B., Ma C., Shen J., Tu J., et al. A large insertion in bHLH transcription factor BrTT8 resulting in yellow seed coat in Brassica rapa. PLoS ONE, 2012, 7: e44145 CrossRef PubMed ADS Google Scholar

[57] Lin R., Ding L., Casola C., Ripoll D.R., Feschotte C., Wang H.. Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science, 2007, 318: 1302-1305 CrossRef PubMed ADS Google Scholar

[58] Lisch D.. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol, 2009, 60: 43-66 CrossRef PubMed Google Scholar

[59] Lisch, D. (2013). How important are transposons for plant evolution? Nat Rev Genet 14, 49–61. Google Scholar

[60] Liu B., Kanazawa A., Matsumura H., Takahashi R., Harada K., Abe J.. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics, 2008, 180: 995-1007 CrossRef PubMed Google Scholar

[61] Liu J., He Y., Amasino R., Chen X.. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev, 2004, 18: 2873-2878 CrossRef PubMed Google Scholar

[62] Long Q., Rabanal F.A., Meng D., Huber C.D., Farlow A., Platzer A., Zhang Q., Vilhjálmsson B.J., Korte A., Nizhynska V., et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet, 2013, 45: 884-890 CrossRef PubMed Google Scholar

[63] Magalhaes J.V., Liu J., Guimarães C.T., Lana U.G.P., Alves V.M.C., Wang Y.H., Schaffert R.E., Hoekenga O.A., Piñeros M.A., Shaff J.E., et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet, 2007, 39: 1156-1161 CrossRef PubMed Google Scholar

[64] Mao H., Wang H., Liu S., Li Z., Yang X., Yan J., Li J., Tran L.S.P., Qin F.. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun, 2015, 6: 8326 CrossRef PubMed ADS Google Scholar

[65] Martienssen R.. Great leap forward? Transposable elements, small interfering RNA and adaptive Lamarckian evolution. New Phytol, 2008, 179: 570-572 CrossRef PubMed Google Scholar

[66] Martienssen R., Barkan A., Taylor W.C., Freeling M.. Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize.. Genes Dev, 1990, 4: 331-343 CrossRef PubMed Google Scholar

[67] Martin A., Troadec C., Boualem A., Rajab M., Fernandez R., Morin H., Pitrat M., Dogimont C., Bendahmane A.. A transposon-induced epigenetic change leads to sex determination in melon. Nature, 2009, 461: 1135-1138 CrossRef PubMed ADS Google Scholar

[68] McCLINTOCK B.. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA, 1950, 36: 344-355 CrossRef PubMed ADS Google Scholar

[69] McClintock B.. Chromosome organization and genic expression. Cold Spring Harbor Symposia Quantitative Biol, 1951, 16: 13-47 CrossRef Google Scholar

[70] McClintock B.. The significance of responses of the genome to challenge. Science, 1984, 226: 792-801 CrossRef PubMed ADS Google Scholar

[71] McCue A.D., Nuthikattu S., Reeder S.H., Slotkin R.K., Kakutani T.. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet, 2012, 8: e1002474 CrossRef PubMed Google Scholar

[72] McCue A.D., Slotkin R.K.. Transposable element small RNAs as regulators of gene expression. Trends Genets, 2012, 28: 616-623 CrossRef PubMed Google Scholar

[73] McDowell J.M., Meyers B.C.. A transposable element is domesticated for service in the plant immune system. Proc Natl Acad Sci USA, 2013, 110: 14821-14822 CrossRef PubMed ADS Google Scholar

[74] Michaels S.D., He Y., Scortecci K.C., Amasino R.M.. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA, 2003, 100: 10102-10107 CrossRef PubMed ADS Google Scholar

[75] Momose M., Abe Y., Ozeki Y.. Miniature Inverted-Repeat Transposable Elements of Stowaway Are Active in Potato. Genetics, 2010, 186: 59-66 CrossRef PubMed Google Scholar

[76] Moon S., Jung K.H., Lee D.E., Jiang W.Z., Koh H.J., Heu M.H., Lee D.S., Suh H.S., An G.. Identification of Active Transposon dTok , a Member of the hAT Family, in Rice. Plant Cell Physiol, 2006, 47: 1473-1483 CrossRef PubMed Google Scholar

[77] Muehlbauer G.J., Bhau B.S., Syed N.H., Heinen S., Cho S., Marshall D., Pateyron S., Buisine N., Chalhoub B., Flavell A.J.. A hAT superfamily transposase recruited by the cereal grass genome. Mol Genet Genomics, 2006, 275: 553-563 CrossRef PubMed Google Scholar

[78] Naito K., Cho E., Yang G., Campbell M.A., Yano K., Okumoto Y., Tanisaka T., Wessler S.R.. Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA, 2006, 103: 17620-17625 CrossRef PubMed ADS Google Scholar

[79] Naito K., Zhang F., Tsukiyama T., Saito H., Hancock C.N., Richardson A.O., Okumoto Y., Tanisaka T., Wessler S.R.. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature, 2009, 461: 1130-1134 CrossRef PubMed ADS Google Scholar

[80] Nakayama H., Afzal M., Okuno K.. Intraspecific differentiation and geographical distribution of Wx alleles for low amylose content in endosperm of foxtail millet, Setaria italica (L.) Beauv. Euphytica, 1998, 102: 289-293 CrossRef Google Scholar

[81] Nakazaki T., Okumoto Y., Horibata A., Yamahira S., Teraishi M., Nishida H., Inoue H., Tanisaka T.. Mobilization of a transposon in the rice genome. Nature, 2003, 421: 170-172 CrossRef PubMed ADS Google Scholar

[82] Ong-Abdullah M., Ordway J.M., Jiang N., Ooi S.E., Kok S.Y., Sarpan N., Azimi N., Hashim A.T., Ishak Z., Rosli S.K., et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature, 2015, 525: 533-537 CrossRef PubMed ADS Google Scholar

[83] Park K.I., Ishikawa N., Morita Y., Choi J.D., Hoshino A., Iida S.. A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation. Plant J, 2007, 49: 641-654 CrossRef PubMed Google Scholar

[84] Paszkowski J.. the karma of oil palms. Nature, 2015, 525: 466-467 CrossRef PubMed ADS Google Scholar

[85] Quadrana L., Almeida J., Asís R., Duffy T., Dominguez P.G., Bermúdez L., Conti G., Corrêa da Silva J.V., Peralta I.E., Colot V., et al. Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Commun, 2014, 5: 3027 CrossRef PubMed ADS Google Scholar

[86] Ratcliffe, O.J., Amaya, I., Vincent, C.A., Rothstein, S., Carpenter, R., Coen, E.S., and Bradley, D.J. (1998). A common mechanism controls the life cycle and architecture of plants. Development 125, 1609–1615. Google Scholar

[87] Rebollo R., Romanish M.T., Mager D.L.. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet, 2012, 46: 21-42 CrossRef PubMed Google Scholar

[88] Salvi S., Sponza G., Morgante M., Tomes D., Niu X., Fengler K.A., Meeley R., Ananiev E.V., Svitashev S., Bruggemann E., et al. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA, 2007, 104: 11376-11381 CrossRef PubMed ADS Google Scholar

[89] Sano Y.. Differential regulation of waxy gene expression in rice endosperm. Theoret Appl Genets, 1984, 68: 467-473 CrossRef PubMed Google Scholar

[90] Saze H., Kakutani T.. Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J, 2007, 26: 3641-3652 CrossRef PubMed Google Scholar

[91] Saze H., Shiraishi A., Miura A., Kakutani T.. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science, 2008, 319: 462-465 CrossRef PubMed ADS Google Scholar

[92] Selinger D.A., Chandler V.L.. B-Bolivia , an Allele of the Maize b1 Gene with Variable Expression, Contains a High Copy Retrotransposon-Related Sequence Immediately Upstream. Plant Physiol, 2001, 125: 1363-1379 CrossRef PubMed Google Scholar

[93] Singh P.K., Bourque G., Craig N.L., Dubnau J.T., Feschotte C., Flasch D.A., Gunderson K.L., Malik H.S., Moran J.V., Peters J.E., et al. Mobile genetic elements and genome evolution 2014. Mobile DNA, 2014, 5: 26 CrossRef PubMed Google Scholar

[94] Slotkin R.K., Martienssen R.. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet, 2007, 8: 272-285 CrossRef PubMed Google Scholar

[95] Slotkin, R.K., Nuthikattu, S., and Jiang, N. (2012). The impact of transposable elements on gene and genome evolution. In: Plant Genome Diversity. Vienna: Springer 35–58. Google Scholar

[96] Smith A.M.. Major differences in isoforms of starch-branching enzyme between developing embryos of round- and wrinkled-seeded peas (Pisum sativum L.). Planta, 1988, 175: 270-279 CrossRef PubMed Google Scholar

[97] Sommer H., Saedler H.. Structure of the chalcone synthase gene of Antirrhinum majus. Molec Gen Genet, 1986, 202: 429-434 CrossRef Google Scholar

[98] Studer A., Zhao Q., Ross-Ibarra J., Doebley J.. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet, 2011, 43: 1160-1163 CrossRef PubMed Google Scholar

[99] Tenaillon M.I., Hollister J.D., Gaut B.S.. A triptych of the evolution of plant transposable elements. Trends Plant Sci, 2010, 15: 471-478 CrossRef PubMed Google Scholar

[100] Tsuchiya T., Eulgem T.. An alternative polyadenylation mechanism coopted to the ArabidopsisRPP7 gene through intronic retrotransposon domestication. Proc Natl Acad Sci USA, 2013, 110: E3535-E3543 CrossRef PubMed ADS Google Scholar

[101] Tsugane K., Maekawa M., Takagi K., Takahara H., Qian Q., Eun C.H., Iida S.. An active DNA transposon nDart causing leaf variegation and mutable dwarfism and its related elements in rice. Plant J, 2006, 45: 46-57 CrossRef PubMed Google Scholar

[102] Uchiyama T., Hiura S., Ebinuma I., Senda M., Mikami T., Martin C., Kishima Y.. A pair of transposons coordinately suppresses gene expression, independent of pathways mediated by siRNA in Antirrhinum. New Phytol, 2013, 197: 431-440 CrossRef PubMed Google Scholar

[103] van der Knaap E., Sanyal A., Jackson S.A., Tanksley S.D.. High-Resolution Fine Mapping and Fluorescence in Situ Hybridization Analysis of sun , a Locus Controlling Tomato Fruit Shape, Reveals a Region of the Tomato Genome Prone to DNA Rearrangements. Genetics, 2004, 168: 2127-2140 CrossRef PubMed Google Scholar

[104] Van Meter M., Kashyap M., Rezazadeh S., Geneva A.J., Morello T.D., Seluanov A., Gorbunova V.. SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age. Nat Commun, 2014, 5: 5011 CrossRef PubMed ADS Google Scholar

[105] Varagona M.J., Purugganan M., Wessler S.R.. Alternative splicing induced by insertion of retrotransposons into the maize waxy gene.. Plant Cell, 1992, 4: 811-820 CrossRef PubMed Google Scholar

[106] Wang K., Huang G., Zhu Y.. Transposable elements play an important role during cotton genome evolution and fiber cell development. Sci China Life Sci, 2016, 59: 112-121 CrossRef PubMed Google Scholar

[107] Wang K., Wang Z., Li F., Ye W., Wang J., Song G., Yue Z., Cong L., Shang H., Zhu S., et al. The draft genome of a diploid cotton Gossypium raimondii. Nat Genet, 2012, 44: 1098-1103 CrossRef PubMed Google Scholar

[108] Wei L., Gu L., Song X., Cui X., Lu Z., Zhou M., Wang L., Hu F., Zhai J., Meyers B.C., et al. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA, 2014, 111: 3877-3882 CrossRef PubMed ADS Google Scholar

[109] Wessler, S.R. (1996). Turned on by stress. Plant retrotransposons. Curr Biol 6, 959–961. Google Scholar

[110] Wessler S.R., Baran G., Varagona M., Dellaporta S.L.. Excision of Ds produces waxy proteins with a range of enzymatic activities.. EMBO J, 1986, 5: 2427-2432 CrossRef Google Scholar

[111] Woodhouse M.R., Cheng F., Pires J.C., Lisch D., Freeling M., Wang X.. Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids. Proc Natl Acad Sci USA, 2014, 111: 5283-5288 CrossRef PubMed ADS Google Scholar

[112] Xiao H., Jiang N., Schaffner E., Stockinger E.J., van der Knaap E.. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science, 2008, 319: 1527-1530 CrossRef PubMed ADS Google Scholar

[113] Xie M., Hong C., Zhang B., Lowdon R.F., Xing X., Li D., Zhou X., Lee H.J., Maire C.L., Ligon K.L., et al. DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat Genet, 2013, 45: 836-841 CrossRef PubMed Google Scholar

[114] Xue W., Xing Y., Weng X., Zhao Y., Tang W., Wang L., Zhou H., Yu S., Xu C., Li X., et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet, 2008, 40: 761-767 CrossRef PubMed Google Scholar

[115] Yan Y., Zhang Y., Yang K., Sun Z., Fu Y., Chen X., Fang R.. Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J, 2011, 65: 820-828 CrossRef PubMed Google Scholar

[116] Yang Q., Li Z., Li W., Ku L., Wang C., Ye J., Li K., Yang N., Li Y., Zhong T., et al. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci USA, 2013, 110: 16969-16974 CrossRef PubMed ADS Google Scholar

[117] Yao J.L., Dong Y.H., Morris B.A.M.. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci USA, 2001, 98: 1306-1311 CrossRef ADS Google Scholar

[118] Yin B.L., Guo L., Zhang D.F., Terzaghi W., Wang X.F., Liu T.T., He H., Cheng Z.K., Deng X.W.. Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol Plant, 2008, 1: 816-829 CrossRef PubMed Google Scholar

[119] Zabala G., Vodkin L.. Novel exon combinations generated by alternative splicing of gene fragments mobilized by a CACTA transposon in Glycine max. BMC Plant Biol, 2007, 7: 38 CrossRef PubMed Google Scholar

[120] Zabala G., Vodkin L.O.. The wp Mutation of Glycine max Carries a Gene-Fragment-Rich Transposon of the CACTA Superfamily. Plant Cell, 2005, 17: 2619-2632 CrossRef PubMed Google Scholar

[121] Zemach A., Kim M.Y., Hsieh P.H., Coleman-Derr D., Eshed-Williams L., Thao K., Harmer S.L., Zilberman D.. The Arabidopsis nucleosome remodeler DDM1 Allows DNA methyltransferases to access H1-containing heterochromatin. Cell, 2013, 153: 193-205 CrossRef PubMed Google Scholar

[122] Zeng F., Cheng B.. Transposable Element Insertion and Epigenetic Modification Cause the Multiallelic Variation in the Expression of FAE1 in Sinapis alba. Plant Cell, 2014, 26: 2648-2659 CrossRef PubMed Google Scholar

[123] Zhai J., Liu J., Liu B., Li P., Meyers B.C., Chen X., Cao X., Ecker J.R.. Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet, 2008, 4: e1000056 CrossRef PubMed Google Scholar

[124] Zhang J., Zhang F., Peterson T.. Transposition of reversed Ac element ends generates novel chimeric genes in maize. PLoS Genet, 2006, 2: e164 CrossRef PubMed Google Scholar

[125] Zhang P., Allen W.B., Nagasawa N., Ching A.S., Heppard E.P., Li H., Hao X., Li X., Yang X., Yan J., et al. A transposable element insertion within ZmGE2 gene is associated with increase in embryo to endosperm ratio in maize. Theor Appl Genet, 2012, 125: 1463-1471 CrossRef PubMed Google Scholar

[126] Zhang T., Hu Y., Jiang W., Fang L., Guan X., Chen J., Zhang J., Saski C.A., Scheffler B.E., Stelly D.M., et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol, 2015, 33: 531-537 CrossRef PubMed Google Scholar

[127] Zhang X.. The epigenetic landscape of plants. Science, 2008, 320: 489-492 CrossRef PubMed ADS Google Scholar

[128] Xianwei S., Zhang X., Sun J., Cao X.F.. Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol, 2015, 169: pp.00836.2015 CrossRef PubMed Google Scholar

  • Figure 1

    Transposable elements (TEs) regulate gene expression by genetic (A–D, blue box) or epigenetic mechanisms (E–H, red box). Black arrowheads represent transcription start sites. Rectangles represent exons (black), introns (white). Black lines indicate the upstream and downstream region of gene body.

  • Figure 2

    Transposable elements (TEs) shape gene regulatory networks by modifying transcription factor binding sites (TFBS). The yellow triangle represents a TE. Rounded rectangles represent TFBS. Orange ellipses represent transcription factors. Black rectangles represent exons and white rectangles represent introns of genes. Black lines indicate the upstream and downstream regions of the gene. The arrowhead represents the transcription start site.

  • Table 1   Effect of TEs on phenotypic variation in plants

    Regulatory mechanism

    TE classification

    Regulated gene

    Plant phenotypes


    Insertional mutagenesis

    *Class II, Ac/Ds


    Variation in pigmentation pattern in maize kernels

    (McClintock, 1950)

    *Class I, LTR, Dasheng


    Rice gold hull and internode (gh) mutants

    (Hong et al., 2012)

    *Class II, CACTA superfamily, Cs1


    Variegated pericarp in sorghum grain

    (Chopra et al., 1999)



    Yellow seed coat in Brassica rapa

    (Li et al., 2012)

    *Class I and Class II


    Flower color variation in morning glory

    (Clegg and Durbin, 2000, 2003)

    *Class II, Mutator


    Pale flowers and ivory seeds in Ipomoea purpurea

    (Park et al., 2007)

    *Class I, Gypsy-type LTR, Gret1


    Changes in grape skin color

    (Kobayashi et al., 2004)

    Class II, MITE


    Changes in potato tuber skin color

    (Momose et al., 2010)

    Class I, LTR, dem1


    Parthenocarpic production of apple fruit

    (Yao et al., 2001)

    *Class II, Ac/Ds


    Waxy kernels in maize

    (Wessler et al., 1986)

    *Class II, Ac/Ds


    Wrinkled-seed character in peas

    (Bhattacharyya et al., 1990)

    *Class I and Class II


    Waxy and low-amylase types of foxtail millet

    (Kawase et al., 2005)

    *Class I, LTR, Dasheng


    Glutinous rice seed in Oragamochi

    (Hori et al., 2007)

    Class II, hAT family, dTok0


    Multiple floral organs and numerous seeds in rice

    (Moon et al., 2006)

    Class II, MuDR


    Increased embryo to endosperm ratio in maize

    (Zhang et al., 2012)

    Regulatory elements

    *Class II, Mu1


    White sectors on maize leaves

    (Martienssen et al., 1990)

    Class II, Harbinger


    Purple cauliflower

    (Chiu et al., 2010)

    Class I, retrotransposon


    Maize seed color

    (Selinger and Chandler, 2001)

    *Class I, LTR, Renovator


    Blast resistance in rice

    (Hayashi and Yoshida, 2009)

    *Class I, Copia family, Hopscotch


    Increased apical dominance in maize

    (Studer et al., 2011)

    *Class II, hAT family, Hatvine1-rrm


    Somatic variation in cluster shape in grapevine

    (Fernandez et al., 2010)

    Class II, MITE


    Flowering time in maize

    (Salvi et al., 2007)

    Class II, MITE


    Aluminum tolerance in sorghum

    (Magalhaes et al., 2007)

    *Class II, MITE, mPing

    Os01g0299700, Os02g0135500, Os02g0582900

    Response to stress in rice

    (Naito et al., 2009)

    *Class I, Copia-like


    The accumulation of anthocyanins in blood oranges

    (Butelli et al., 2012)

    *Class I, LTR


    Waxy kernels in maize

    (Varagona et al., 1992)

    *Class I, Copia-like, COPIA-R7


    Pathogen responses

    (Tsuchiya and Eulgem, 2013)

    *Class II, CACTA family


    Flower color and seed coat in soybean

    (Zabala and Vodkin, 2007; Zabala and Vodkin, 2005)

    Rearrangement of gene structures

    *Class II, Ac


    Orange pericarp and cob in maize

    (Zhang et al., 2006)

    *Class I, Copia-like, Rider


    Morphological variation of tomato fruit

    (Xiao et al., 2008)

    *Class II, hAT family,Tam3

    nivea (niv)

    Petal color in Antirrhinum

    (Coen et al., 1986; Uchiyama et al., 2013)

    Domesticated transposase genes

    *Class II, MULE

    FHY3, FAR1

    Response to light signaling in Arabidopsis

    (Lin et al., 2007)

    *Class II, MULE


    Severe developmental defects in Arabidopsis

    (Cowan et al., 2005; Joly-Lopez et al., 2012)

    *Class II, hAT-like TE


    Essential for plant development in Arabidopsis

    (Bundock and Hooykaas, 2005)

    Epigenetic regulation

    Class I, SINE


    Late-flowering in Arabidopsis

    (Fujimoto et al., 2008; Kinoshita et al., 2007)

    *Class II, MULE


    Late-flowering in Arabidopsis

    (Liu et al., 2004)

    *Class I, LINE


    Severe dwarfing in Arabidopsis

    (Saze and Kakutani, 2007; Saze et al., 2008)

    Class II, hAT family, nDart1


    Pale-yellow variegated leaves in rice seedlings

    (Tsugane et al., 2006)

    *Class II, hAT family, Gyno-hAT


    Sex determination in melon

    (Martin et al., 2009)

    *Class I, Copia-like, SORE-1


    Photoperiod insensitivity in soybean.

    (Kanazawa et al., 2009)

    *Class II, CACTA


    Attenuated photoperiod sensitivity in maize

    (Yang et al., 2013)

    *Class I, SINE


    Vitamin E accumulation in tomato fruits

    (Quadrana et al., 2014)

    *Class I, Copia-like, Sal-T1


    Erucic contents in yellow mustard (Sinapis alba)

    (Zeng and Cheng, 2014)

    (To be continued on the next page)


    Regulatory mechanism

    TE classification

    Regulated gene

    Plant phenotypes


    Epigenetic regulation

    *Class I, Karma


    Mantled fruits in oil palm.

    (Ong-Abdullah et al., 2015)

    *Class I, LTR, Athila family


    Stress-sensitivity in Arabidopsis

    (McCue et al., 2012)

    *Class II, MITE


    ABA signaling and abiotic stress responses in rice

    (Yan et al., 2011)

    *Class II, MITE, En/Spm-like

    CYP76M7, OsKSL7, CYP99A3, OsCPS4, EUI

    Plant height in rice

    (Wei et al., 2014)

    *Class II, MITE

    OsGSR1, OsBR6ox

    Leaf angle in rice

    (Wei et al., 2014)

    *Class II, MITE


    Natural variation in maize drought tolerance

    (Mao et al., 2015)

    *Class II, MITE


    Leaf Angle and Seed Size in Rice

    (Zhang et al., 2015b)

    *: These examples are discussed in this review.

Copyright 2020 Science China Press Co., Ltd. 《中国科学》杂志社有限责任公司 版权所有

京ICP备17057255号       京公网安备11010102003388号