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

Science China Life Sciences

Volumn 59, Issue 1, 2016, Pages 24-37

  Wei, Liya ^a   Cao, Xiaofeng ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

gene expression; phenotypic variation; transposable elements

Indexed keywords

PLANT RNA; TRANSPOSON;

GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; GENETIC SELECTION; GENETIC VARIATION; GENETICS; HUMAN; PHENOTYPE; PLANT; PLANT GENOME; REGULATORY SEQUENCE; TRANSPOSON;

DNA TRANSPOSABLE ELEMENTS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENE REARRANGEMENT; GENE REGULATORY NETWORKS; GENETIC VARIATION; GENOME, PLANT; HUMANS; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PLANTS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA, PLANT; SELECTION, GENETIC;

EID: 84956946039     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-015-4993-2     Document Type: Review

References (128)

1. Adam, H., Jouannic, S., Orieux, Y., Morcillo, F., Richaud, F., Duval, Y., and Tregear, J.W. (2007). Functional characterization of MADS box genes involved in the determination of oil palm flower structure. J Exp Bot 58, 1245–1259.
2. Barkan, A., Miles, D., and Taylor, W.C. (1986). Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J 5, 1421–1427.
3. Beló, A., Nobuta, K., Venu, R.C., Janardhanan, P., Wang, G.L., and Meyers, B. (2008). Transposable element regulation in rice and Arabidopsis: diverse patterns of active expression and siRNA-mediated silencing. Tropical Plant Biol 1, 72–84.
4. Bhattacharyya, M.K., Smith, A.M., Ellis, T.H., Hedley, C., and Martin, C. (1990). The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell 60, 115–122.
5. Boss, P.K., Sreekantan, L., and Thomas, M.R. (2006). A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct Plant Biol 33, 31–41.
6. Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R., and Coen, E. (1997). Inflorescence commitment and architecture in Arabidopsis. Science 275, 80–83.
7. Bundock, P., and Hooykaas, P. (2005). An Arabidopsis hAT-like transposase is essential for plant development. Nature 436, 282–284.
8. Butelli, E., Licciardello, C., Zhang, Y., Liu, J., Mackay, S., Bailey, P., Reforgiato-Recupero, G., and Martin, C. (2012). Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24, 1242–1255.
9. Chen, S.M., and Coe, E.H., Jr. (1977). Control of anthocyanin synthesis by the C locus in maize. Biochem Genet 15, 333–346.
10. Cheng, Z., Buell, C.R., Wing, R.A., Gu, M., and Jiang, J. (2001). Toward a cytological characterization of the rice genome. Genome Res 11, 2133–2141.
11. Chiu, L.W., Zhou, X., Burke, S., Wu, X., Prior, R.L., and Li, L. (2010). The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiol 154, 1470–1480.
12. Chopra, S., Brendel, V., Zhang, J., Axtell, J.D., and Peterson, T. (1999). Molecular characterization of a mutable pigmentation phenotype and isolation of the first active transposable element from Sorghum bicolor. Proc Natl Acad Sci USA 96, 15330–15335.
13. Clegg, M.T., and Durbin, M.L. (2000). Flower color variation: a model for the experimental study of evolution. Proc Natl Acad Sci USA 97, 7016–7023.
14. Clegg, M.T., and Durbin, M.L. (2003). Tracing floral adaptations from ecology to molecules. Nat Rev Genet 4, 206–215.
15. Coen, E.S., Carpenter, R., and Martin, C. (1986). Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell 47, 285–296.
16. Cordaux, R., and Batzer, M.A. (2009). The impact of retrotransposons on human genome evolution. Nat Rev Genet 10, 691–703.
17. Cowan, R.K., Hoen, D.R., Schoen, D.J., and Bureau, T.E. (2005). MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol 22, 2084–2089.
18. Cubas, P., Lauter, N., Doebley, J., and Coen, E. (1999). The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18, 215–222.
19. Cui, X., and Cao, X. (2014). Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21c, 83–88.
20. Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., An, G., and Cao, X. (2013). Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci USA 110, 1953–1958.
21. Ding, Y., Wang, X., Su, L., Zhai, J., Cao, S., Zhang, D., Liu, C., Bi, Y., Qian, Q., Cheng, Z., Chu, C., and Cao, X. (2007). SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19, 9–22.
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.
23. Erwin, J.A., Marchetto, M.C., and Gage, F.H. (2014). Mobile DNA elements in the generation of diversity and complexity in the brain. Nat Rev Neurosci 15, 497–506.
24. Fernandez, L., Torregrosa, L., Segura, V., Bouquet, A., and Martinez-Zapater, J.M. (2010). Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J 61, 545–557.
25. Feschotte, C. (2008). Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9, 397–405.
26. Feschotte, C., Jiang, N., and Wessler, S.R. (2002). Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3, 329–341.
27. Fransz, P., Armstrong, S., Alonso-Blanco, C., Fischer, T.C., Torres-Ruiz, R.A., and Jones, G. (1998). Cytogenetics for the model system Arabidopsis thaliana. Plant J 13, 867–876.
28. Fujimoto, R., Kinoshita, Y., Kawabe, A., Kinoshita, T., Takashima, K., Nordborg, M., Nasrallah, M.E., Shimizu, K.K., Kudoh, H., and Kakutani, T. (2008). Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet 4, e1000048.
29. Gazzani, S., Gendall, A.R., Lister, C., and Dean, C. (2003). Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132, 1107–1114.
30. Hancks, D.C., and Kazazian, H.H., Jr. (2012). Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22, 191–203.
31. Hayashi, K., and Yoshida, H. (2009). Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J 57, 413–425.
32. Hiltbrunner, A., Tscheuschler, A., Viczian, A., Kunkel, T., Kircher, S., and Schafer, E. (2006). FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant Cell Physiol 47, 1023–1034.
33. Hiltbrunner, A., Viczian, A., Bury, E., Tscheuschler, A., Kircher, S., Toth, R., Honsberger, A., Nagy, F., Fankhauser, C., and Schafer, E. (2005). Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr Biol 15, 2125–2130.
34. Hong, L., Qian, Q., Tang, D., Wang, K., Li, M., and Cheng, Z. (2012). A mutation in the rice chalcone isomerase gene causes the golden hull and internode 1 phenotype. Planta 236, 141–151.
35. Hori, Y., Fujimoto, R., Sato, Y., and Nishio, T. (2007). A novel wx mutation caused by insertion of a retrotransposon-like sequence in a glutinous cultivar of rice (Oryza sativa). Theor Appl Genet 115, 217–224.
36. Huang, C.R., Burns, K.H., and Boeke, J.D. (2012). Active transposition in genomes. Annu Rev Genet 46, 651–675.
37. Javidfar, F., and Cheng, B. (2013). Single locus, multiallelic inheritance of erucic acid content and linkage mapping of gene in yellow mustard. Crop Sci 53, 825–832.
38. Jeong, J.S., Kim, Y.S., Baek, K.H., Jung, H., Ha, S.H., Do Choi, Y., Kim, M., Reuzeau, C., and Kim, J.K. (2010). Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153, 185–197.
39. Jiang, N., Bao, Z., Zhang, X., Hirochika, H., Eddy, S.R., McCouch, S.R., and Wessler, S.R. (2003). An active DNA transposon family in rice. Nature 421, 163–167.
40. Jiang, N., Feschotte, C., Zhang, X., and Wessler, S.R. (2004). Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7, 115–119.
41. Joly-Lopez, Z., Forczek, E., Hoen, D.R., Juretic, N., and Bureau, T.E. (2012). A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet 8, e1002931.
42. Kaer, K., and Speek, M. (2013). Retroelements in human disease. Gene 518, 231–241.
43. Kanazawa, A., Liu, B., Kong, F., Arase, S., and 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.
44. Kawase, M., Fukunaga, K., and Kato, K. (2005). Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol Genet Genomics 274, 131–140.
45. Kazazian, H.H., Jr., Wong, C., Youssoufian, H., Scott, A.F., Phillips, D.G., and Antonarakis, S.E. (1988). Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 332, 164–166.
46. Kikuchi, K., Terauchi, K., Wada, M., and Hirano, H.Y. (2003). The plant MITE mPing is mobilized in anther culture. Nature 421, 167–170.
47. Kinoshita, Y., Saze, H., Kinoshita, T., Miura, A., Soppe, W.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.
48. Kiyosawa, S. (1972). The inheritance of blast resistance transferred from some indica varieties in rice. Bull Nat Inst Agric Sci 23, 69–96.
49. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H. (2004). Retrotransposon-induced mutations in grape skin color. Science 304, 982.
50. Kunarso, G., Chia, N.-Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y.-S., Ng, H.-H., and Bourque, G. (2010). Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42, 631–634.
51. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., LeVine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J.P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, P., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J.C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R.H., Wilson, R.K., Hillier, L.W., McPherson, J.D., Marra, M.A., Mardis, E.R., Fulton, L.A., Chinwalla, A.T., Pepin, K.H., Gish, W.R., Chissoe, S.L., Wendl, M.C., Delehaunty, K.D., Miner, T.L., Delehaunty, A., Kramer, J.B., Cook, L.L., Fulton, R.S., Johnson, D.L., Minx, P.J., Clifton, S.W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J.F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., Gibbs, R.A., Muzny, D.M., Scherer, S.E., Bouck, J.B., Sodergren, E.J., Worley, K.C., Rives, C.M., Gorrell, J.H., Metzker, M.L., Naylor, S.L., Kucherlapati, R.S., Nelson, D.L., Weinstock, G.M., Sakaki, Y., Fujiyama, A., Hattori, M., Yada, T., Toyoda, A., Itoh, T., Kawagoe, C., Watanabe, H., Totoki, Y., Taylor, T., Weissenbach, J., Heilig, R., Saurin, W., Artiguenave, F., Brottier, P., Bruls, T., Pelletier, E., Robert, C., Wincker, P., Smith, D.R., Doucette-Stamm, L., Rubenfield, M., Weinstock, K., Lee, H.M., Dubois, J., Rosenthal, A., Platzer, M., Nyakatura, G., Taudien, S., Rump, A., Yang, H., Yu, J., Wang, J., Huang, G., Gu, J., Hood, L., Rowen, L., Madan, A., Qin, S., Davis, R.W., Federspiel, N.A., Abola, A.P., Proctor, M.J., Myers, R.M., Schmutz, J., Dickson, M., Grimwood, J., Cox, D.R., Olson, M.V., Kaul, R., Raymond, C., Shimizu, N., Kawasaki, K., Minoshima, S., Evans, G.A., Athanasiou, M., Schultz, R., Roe, B.A., Chen, F., Pan, H., Ramser, J., Lehrach, H., Reinhardt, R., McCombie, W.R., de la Bastide, M., Dedhia, N., Blocker, H., Hornischer, K., Nordsiek, G., Agarwala, R., Aravind, L., Bailey, J.A., Bateman, A., Batzoglou, S., Birney, E., Bork, P., Brown, D.G., Burge, C.B., Cerutti, L., Chen, H.C., Church, D., Clamp, M., Copley, R.R., Doerks, T., Eddy, S.R., Eichler, E.E., Furey, T.S., Galagan, J., Gilbert, J.G., Harmon, C., Hayashizaki, Y., Haussler, D., Hermjakob, H., Hokamp, K., Jang, W., Johnson, L.S., Jones, T.A., Kasif, S., Kaspryzk, A., Kennedy, S., Kent, W.J., Kitts, P., Koonin, E.V., Korf, I., Kulp, D., Lancet, D., Lowe, T.M., McLysaght, A., Mikkelsen, T., Moran, J.V., Mulder, N., Pollara, V.J., Ponting, C.P., Schuler, G., Schultz, J., Slater, G., Smit, A.F., Stupka, E., Szustakowski, J., Thierry-Mieg, D., Thierry-Mieg, J., Wagner, L., Wallis, J., Wheeler, R., Williams, A., Wolf, Y.I., Wolfe, K.H., Yang, S.P., Yeh, R.F., Collins, F., Guyer, M.S., Peterson, J., Felsenfeld, A., Wetterstrand, K.A., Patrinos, A., Morgan, M.J., de Jong, P., Catanese, J.J., Osoegawa, K., Shizuya, H., Choi, S., Chen, Y.J., and International Human Genome Sequencing, C. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860–921.
52. Levin, H.L., and Moran, J.V. (2011). Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12, 615–627.
53. Li, F., Fan, G., Lu, C., Xiao, G., Zou, C., Kohel, R.J., Ma, Z., Shang, H., Ma, X., Wu, J., Liang, X., Huang, G., Percy, R.G., Liu, K., Yang, W., Chen, W., Du, X., Shi, C., Yuan, Y., Ye, W., Liu, X., Zhang, X., Liu, W., Wei, H., Wei, S., Huang, G., Zhang, X., Zhu, S., Zhang, H., Sun, F., Wang, X., Liang, J., Wang, J., He, Q., Huang, L., Wang, J., Cui, J., Song, G., Wang, K., Xu, X., Yu, J.Z., Zhu, Y., and Yu, S. (2015). Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33, 524–530.
54. Li, F., Fan, G., Wang, K., Sun, F., Yuan, Y., Song, G., Li, Q., Ma, Z., Lu, C., Zou, C., Chen, W., Liang, X., Shang, H., Liu, W., Shi, C., Xiao, G., Gou, C., Ye, W., Xu, X., Zhang, X., Wei, H., Li, Z., Zhang, G., Wang, J., Liu, K., Kohel, R.J., Percy, R.G., Yu, J.Z., Zhu, Y.X., Wang, J., and Yu, S. (2014a). Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46, 567–572.
55. Li, Q., Xiao, G., and Zhu, Y.X. (2014b). Single-nucleotide resolution mapping of the Gossypium raimondii transcriptome reveals a new mechanism for alternative splicing of introns. Mol Plant 7, 829–840.
56. Li, X., Chen, L., Hong, M., Zhang, Y., Zu, F., Wen, J., Yi, B., Ma, C., Shen, J., Tu, J., and Fu, T. (2012). A large insertion in bHLH transcription factor BrTT8 resulting in yellow seed coat in Brassica rapa. PLoS One 7, e44145.
57. Lin, R., Ding, L., Casola, C., Ripoll, D.R., Feschotte, C., and Wang, H. (2007). Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318, 1302–1305.
58. Lisch, D. (2009). Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60, 43–66.
59. Lisch, D. (2013). How important are transposons for plant evolution? Nat Rev Genet 14, 49–61.
60. Liu, B., Kanazawa, A., Matsumura, H., Takahashi, R., Harada, K., and Abe, J. (2008). Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180, 995–1007.
61. Liu, J., He, Y., Amasino, R., and Chen, X. (2004). siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 18, 2873–2878.
62. Long, Q., Rabanal, F.A., Meng, D., Huber, C.D., Farlow, A., Platzer, A., Zhang, Q., Vilhjalmsson, B.J., Korte, A., Nizhynska, V., Voronin, V., Korte, P., Sedman, L., Mandakova, T., Lysak, M.A., Seren, U., Hellmann, I., and Nordborg, M. (2013). Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet 45, 884–890.
63. Magalhaes, J.V., Liu, J., Guimaraes, C.T., Lana, U.G., Alves, V.M., Wang, Y.H., Schaffert, R.E., Hoekenga, O.A., Pineros, M.A., Shaff, J.E., Klein, P.E., Carneiro, N.P., Coelho, C.M., Trick, H.N., and Kochian, L.V. (2007). A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39, 1156–1161.
64. Mao, H., Wang, H., Liu, S., Li, Z., Yang, X., Yan, J., Li, J., Tran, L.-S.P., and Qin, F. (2015). A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6, 8326.
65. Martienssen, R. (2008). Great leap forward? Transposable elements, small interfering RNA and adaptive Lamarckian evolution. New Phytol 179, 570–572.
66. Martienssen, R., Barkan, A., Taylor, W.C., and Freeling, M. (1990). Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize. Genes Dev 4, 331–343.
67. Martin, A., Troadec, C., Boualem, A., Rajab, M., Fernandez, R., Morin, H., Pitrat, M., Dogimont, C., and Bendahmane, A. (2009). A transposon- induced epigenetic change leads to sex determination in melon. Nature 461, 1135–1138.
68. McClintock, B. (1950). The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36, 344–355.
69. McClintock, B. (1951). Chromosome organization and genic expression. Cold Spring Harbor Symposia on Quantitative Biology 16, 13–47.
70. McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226, 792–801.
71. McCue, A.D., Nuthikattu, S., Reeder, S.H., and Slotkin, R.K. (2012). Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet 8, e1002474.
72. McCue, A.D., and Slotkin, R.K. (2012). Transposable element small RNAs as regulators of gene expression. Trends Genet 28, 616–623.
73. McDowell, J.M., and Meyers, B.C. (2013). A transposable element is domesticated for service in the plant immune system. Proc Natl Acad Sci USA 110, 14821–14822.
74. Michaels, S.D., He, Y., Scortecci, K.C., and Amasino, R.M. (2003). Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100, 10102–10107.
75. Momose, M., Abe, Y., and Ozeki, Y. (2010). Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 186, 59–66.
76. Moon, S., Jung, K.H., Lee, D.E., Jiang, W.Z., Koh, H.J., Heu, M.H., Lee, D.S., Suh, H.S., and An, G. (2006). Identification of active transposon dTok, a member of the hAT family, in rice. Plant Cell Physiol 47, 1473–1483.
77. Muehlbauer, G.J., Bhau, B.S., Syed, N.H., Heinen, S., Cho, S., Marshall, D., Pateyron, S., Buisine, N., Chalhoub, B., and Flavell, A.J. (2006). A hAT superfamily transposase recruited by the cereal grass genome. Mol Genet Genomics 275, 553–563.
78. Naito, K., Cho, E., Yang, G., Campbell, M.A., Yano, K., Okumoto, Y., Tanisaka, T., and Wessler, S.R. (2006). Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103, 17620–17625.
79. 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.
80. Nakayama, H., Afzal, M., and Okuno, K. (1998). Intraspecific differentiation and geographical distribution of Wx alleles for low amylose content in endosperm of foxtail millet, Setaria italica (L.) Beauv. Euphytica 102, 289–293.
81. Nakazaki, T., Okumoto, Y., Horibata, A., Yamahira, S., Teraishi, M., Nishida, H., Inoue, H., and Tanisaka, T. (2003). Mobilization of a transposon in the rice genome. Nature 421, 170–172.
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., Malike, F.A., Bakar, N.A., Marjuni, M., Abdullah, N., Yaakub, Z., Amiruddin, M.D., Nookiah, R., Singh, R., Low, E.L., Chan, K.L., Azizi, N., Smith, S.W., Bacher, B., Budiman, M.A., Van Brunt, A., Wischmeyer, C., Beil, M., Hogan, M., Lakey, N., Lim, C.C., Arulandoo, X., Wong, C.K., Choo, C.N., Wong, W.C., Kwan, Y.Y., Alwee, S.S., Sambanthamurthi, R., and Martienssen, R.A. (2015). Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537
83. Park, K.I., Ishikawa, N., Morita, Y., Choi, J.D., Hoshino, A., and Iida, S. (2007). 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 641–654.
84. Paszkowski, J. (2015). Epigenetics: the karma of oil palms. Nature 525, 466–467
85. Quadrana, L., Almeida, J., Asis, R., Duffy, T., Dominguez, P.G., Bermudez, L., Conti, G., Correa da Silva, J.V., Peralta, I.E., Colot, V., Asurmendi, S., Fernie, A.R., Rossi, M., and Carrari, F. (2014). Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Commun 5, 3027.
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.
87. Rebollo, R., Romanish, M.T., and Mager, D.L. (2012). Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46, 21–42.
88. Salvi, S., Sponza, G., Morgante, M., Tomes, D., Niu, X., Fengler, K.A., Meeley, R., Ananiev, E.V., Svitashev, S., Bruggemann, E., Li, B., Hainey, C.F., Radovic, S., Zaina, G., Rafalski, J.A., Tingey, S.V., Miao, G.H., Phillips, R.L., and Tuberosa, R. (2007). Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104, 11376–11381.
89. Sano, Y. (1984). Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet 68, 467–473.
90. Saze, H., and Kakutani, T. (2007). Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J 26, 3641–3652.
91. Saze, H., Shiraishi, A., Miura, A., and Kakutani, T. (2008). Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319, 462–465.
92. Selinger, D.A., and Chandler, V.L. (2001). B-Bolivia, an allele of the maize b1 gene with variable expression, contains a high copy retrotransposon- related sequence immediately upstream. Plant Physiol 125, 1363–1379.
93. Singh, P., Bourque, G., Craig, N., Dubnau, J., Feschotte, C., Flasch, D., Gunderson, K., Malik, H., Moran, J., Peters, J., Slotkin, R., and Levin, H. (2014). Mobile genetic elements and genome evolution 2014. Mobile DNA 5, 26.
94. Slotkin, R.K., and Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8, 272–285.
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.
96. Smith, A.M. (1988). Major differences in isoforms of starch-branching enzyme between developing embryos of round- and wrinkled-seeded peas (Pisum sativum L.). Planta 175, 270–279.
97. Sommer, H., and Saedler, H. (1986). Structure of the chalcone synthase gene of Antirrhinum majus. Mol Gen Genet 202, 429–434.
98. Studer, A., Zhao, Q., Ross-Ibarra, J., and Doebley, J. (2011). Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43, 1160–1163.
99. Tenaillon, M.I., Hollister, J.D., and Gaut, B.S. (2010). A triptych of the evolution of plant transposable elements. Trends Plant Sci 15, 471–478.
100. Tsuchiya, T., and Eulgem, T. (2013). An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc Natl Acad Sci USA 110, E3535–E3543.
101. Tsugane, K., Maekawa, M., Takagi, K., Takahara, H., Qian, Q., Eun, C.H., and Iida, S. (2006). An active DNA transposon nDart causing leaf variegation and mutable dwarfism and its related elements in rice. Plant J 45, 46–57.
102. Uchiyama, T., Hiura, S., Ebinuma, I., Senda, M., Mikami, T., Martin, C., and Kishima, Y. (2013). A pair of transposons coordinately suppresses gene expression, independent of pathways mediated by siRNA in Antirrhinum. The New phytologist 197, 431–440.
103. van der Knaap, E., Sanyal, A., Jackson, S.A., and Tanksley, S.D. (2004). 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 168, 2127–2140.
104. Van Meter, M., Kashyap, M., Rezazadeh, S., Geneva, A.J., Morello, T.D., Seluanov, A., and Gorbunova, V. (2014). SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age. Nat Commun 5, 5011.
105. 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.
106. Wang, K., Huang, G., and Zhu, Y.X. (2016). Transposable elements play an important role during cotton genome evolution and fiber cell development. Sci China Life Sci doi: 10.1007/s11427-015-4928-y
107. Wang, K., Wang, Z., Li, F., Ye, W., Wang, J., Song, G., Yue, Z., Cong, L., Shang, H., Zhu, S., Zou, C., Li, Q., Yuan, Y., Lu, C., Wei, H., Gou, C., Zheng, Z., Yin, Y., Zhang, X., Liu, K., Wang, B., Song, C., Shi, N., Kohel, R.J., Percy, R.G., Yu, J.Z., Zhu, Y.X., Wang, J., and Yu, S. (2012). The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44, 1098–1103.
108. Wei, L., Gu, L., Song, X., Cui, X., Lu, Z., Zhou, M., Wang, L., Hu, F., Zhai, J., Meyers, B.C., and Cao, X. (2014). Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA 111, 3877–3882.
109. Wessler, S.R. (1996). Turned on by stress. Plant retrotransposons. Curr Biol 6, 959–961.
110. Wessler, S.R., Baran, G., Varagona, M., and Dellaporta, S.L. (1986). Excision of Ds produces waxy proteins with a range of enzymatic activities. EMBO J 5, 2427–2432.
111. Woodhouse, M.R., Cheng, F., Pires, J.C., Lisch, D., Freeling, M., and Wang, X. (2014). Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids. Proc Natl Acad Sci USA 111, 5283–5288.
112. Xiao, H., Jiang, N., Schaffner, E., Stockinger, E.J., and van der Knaap, E. (2008). A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319, 1527–1530.
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., Gascard, P., Sigaroudinia, M., Tlsty, T.D., Kadlecek, T., Weiss, A., O’Geen, H., Farnham, P.J., Madden, P.A.F., Mungall, A.J., Tam, A., Kamoh, B., Cho, S., Moore, R., Hirst, M., Marra, M.A., Costello, J.F., and Wang, T. (2013). DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat Genet 45, 836–841.
114. Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C., Li, X., and Zhang, Q. (2008). Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40, 761–767.
115. Yan, Y., Zhang, Y., Yang, K., Sun, Z., Fu, Y., Chen, X., and Fang, R. (2011). Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J 65, 820–828.
116. Yang, Q., Li, Z., Li, W., Ku, L., Wang, C., Ye, J., Li, K., Yang, N., Li, Y., Zhong, T., Li, J., Chen, Y., Yan, J., Yang, X., and Xu, M. (2013). CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci USA 110, 16969–16974.
117. Yao, J., Dong, Y., and Morris, B.A. (2001). Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci USA 98, 1306–1311.
118. Yin, B.L., Guo, L., Zhang, D.F., Terzaghi, W., Wang, X.F., Liu, T.T., He, H., Cheng, Z.K., and Deng, X.W. (2008). Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol Plant 1, 816–829.
119. 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.
120. Zabala, G., and Vodkin, L.O. (2005). The wp mutation of Glycine max carries a gene-fragment-rich transposon of the CACTA superfamily. Plant Cell 17, 2619–2632.
121. Zemach, A., Kim, M.Y., Hsieh, P.H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, Stacey L., and Zilberman, D. (2013). The Arabidopsis nucleosome remodeler DDM1 Allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205.
122. Zeng, F., and Cheng, B. (2014). Transposable element insertion and epigenetic modification cause the multiallelic variation in the expression of FAE1 in Sinapis alba. Plant Cell 26, 2648–2659.
123. Zhai, J., Liu, J., Liu, B., Li, P., Meyers, B.C., Chen, X., and Cao, X. (2008). Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet 4, e1000056.
124. Zhang, J., Zhang, F., and Peterson, T. (2006). Transposition of reversed Ac element ends generates novel chimeric genes in maize. PLoS Genet 2, e164.
125. Zhang, P., Allen, W.B., Nagasawa, N., Ching, A.S., Heppard, E.P., Li, H., Hao, X., Li, X., Yang, X., Yan, J., Nagato, Y., Sakai, H., Shen, B., and Li, J. (2012). A transposable element insertion within ZmGE2 gene is associated with increase in embryo to endosperm ratio in maize. Theor Appl Genet 125, 1463–1471.
126. Zhang, T., Hu, Y., Jiang, W., Fang, L., Guan, X., Chen, J., Zhang, J., Saski, C.A., Scheffler, B.E., Stelly, D.M., Hulse-Kemp, A.M., Wan, Q., Liu, B., Liu, C., Wang, S., Pan, M., Wang, Y., Wang, D., Ye, W., Chang, L., Zhang, W., Song, Q., Kirkbride, R.C., Chen, X., Dennis, E., Llewellyn, D.J., Peterson, D.G., Thaxton, P., Jones, D.C., Wang, Q., Xu, X., Zhang, H., Wu, H., Zhou, L., Mei, G., Chen, S., Tian, Y., Xiang, D., Li, X., Ding, J., Zuo, Q., Tao, L., Liu, Y., Li, J., Lin, Y., Hui, Y., Cao, Z., Cai, C., Zhu, X., Jiang, Z., Zhou, B., Guo, W., Li, R., and Chen, Z.J. (2015a). Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33, 531–537.
127. Zhang, X. (2008). The epigenetic landscape of plants. Science 320, 489–492.
128. Zhang, X., Sun, J., Cao, X., and Song, X. (2015b). Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol 169, 2118–2128.