No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

and Transposons

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • HTML
    210.94 Kb
  • XML
    181.70 Kb
  • PDF
    811.73 Kb
  • Author: Damon Lisch1
  • Editors: Mick Chandler2, Nancy Craig3
    Affiliations: 1: Purdue University, West Lafayette, IN; 2: Université Paul Sabatier, Toulouse, France; 3: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
  • Received 10 June 2014 Accepted 22 October 2014 Published 05 March 2015
  • Damon Lisch, [email protected]
image of <span class="jp-italic">Mutator</span> and <span class="jp-italic">MULE</span> Transposons
    Preview this microbiology spectrum article:
    Zoom in

    and Transposons, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0032-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0032-2014-2.gif
  • Abstract:

    The system of transposable elements (TEs) is a highly mutagenic family of transposons in maize. Because they transpose at high rates and target genic regions, these transposons can rapidly generate large numbers of new mutants, which has made the system a favored tool for both forward and reverse mutagenesis in maize. Low copy number versions of this system have also proved to be excellent models for understanding the regulation and behavior of Class II transposons in plants. Notably, the availability of a naturally occurring locus that can heritably silence autonomous elements has provided insights into the means by which otherwise active transposons are recognized and silenced. This chapter will provide a review of the biology, regulation, evolution and uses of this remarkable transposon system, with an emphasis on recent developments in our understanding of the ways in which this TE system is recognized and epigenetically silenced as well as recent evidence that -like elements (s) have had a significant impact on the evolution of plant genomes.

  • Citation: Lisch D. 2015. and Transposons. Microbiol Spectrum 3(2):MDNA3-0032-2014. doi:10.1128/microbiolspec.MDNA3-0032-2014.


1. Robertson DS. 1978. Characterization of a mutator system in maize. Mutat Res 51:21–28. [CrossRef]
2. Walbot V. 1991. The Mutator transposable element family of maize. Genet Eng (N Y) 13:1–37. [PubMed][CrossRef]
3. Alleman M, Freeling M. 1986. The Mu transposable elements of maize: evidence for transposition and copy number regulation during development. Genetics 112:107–119. [PubMed]
4. Walbot V, Warren C. 1988. Regulation of Mu element copy number in maize lines with an active or inactive Mutator transposable element system. Mol Gen Genet 211:27–34. [PubMed][CrossRef]
5. Cresse AD, Hulbert SH, Brown WE, Lucas JR, Bennetzen JL. 1995. Mu1-related transposable elements of maize preferentially insert into low copy number DNA. Genetics 140:315–324. [PubMed]
6. McCarty D, Meeley R. 2009. Transposon resources for forward and reverse genetics in maize, p 561–584. In Bennetzen J, Hake S (ed), Handbook of Maize: Genetics and Genomics. Springer, Berlin. [CrossRef]
7. Lisch D. 2002. Mutator transposons. Trends Plant Sci 7:498–504. [PubMed][CrossRef]
8. Lisch D, Jiang H. 2009. Mutator and MULE transposons, p 277–306. In Bennetzen J, Hake S (ed), Handbook of Maize: Genetics and Genomics. Springer, Berlin. [CrossRef]
9. Chomet P, Lisch D, Hardeman KJ, Chandler VL, Freeling M. 1991. Identification of a regulatory transposon that controls the Mutator transposable element system in maize. Genetics 129:261–270. [PubMed]
10. Hershberger RJ, Warren CA, Walbot V. 1991. Mutator activity in maize correlates with the presence and expression of the Mu transposable element Mu9. Proc Natl Acad Sci U S A 88:10198–10202. [PubMed][CrossRef]
11. Qin M, Robertson DS, Ellingboe AH. 1991. Cloning of the mutator transposable element MuA2, a putative regulator of somatic mutability of the a1-Mum2 allele in maize. Genetics 129:845–854. [PubMed]
12. Lisch DR, Freeling M, Langham RJ, Choy MY. 2001. Mutator transposase is widespread in the grasses. Plant Physiol 125:1293–1303. [PubMed][CrossRef]
13. Hershberger RJ, Benito MI, Hardeman KJ, Warren C, Chandler VL, Walbot V. 1995. Characterization of the major transcripts encoded by the regulatory MuDR transposable element of maize. Genetics 140:1087–1098. [PubMed]
14. Kim SH, Walbot V. 2003. Deletion derivatives of the MuDR regulatory transposon of maize encode antisense transcripts but are not dominant-negative regulators of mutator activities. Plant Cell 15:2430–2447. [PubMed][CrossRef]
15. Lisch D, Girard L, Donlin M, Freeling M. 1999. Functional analysis of deletion derivatives of the maize transposon MuDR delineates roles for the MURA and MURB proteins. Genetics 151:331–341. [PubMed]
16. Joanin P, Hershberger RJ, Benito MI, Walbot V. 1997. Sense and antisense transcripts of the maize MuDR regulatory transposon localized by in situ hybridization. Plant Mol Biol 33:23–36. [PubMed][CrossRef]
17. Walbot V, Rudenko GN. 2002. MuDR/Mu transposable elements of maize, Vol 533–564. In Craig NL, Craigie R, Gellert M, Lambowitz AM (ed), Mobile DNA II. ASM Press, Washington DC.
18. Ono A, Kim SH, Walbot V. 2002. Subcellular localization of MURA and MURB proteins encoded by the maize MuDR transposon. Plant Mol Biol 50:599–611. [PubMed][CrossRef]
19. Benito MI, Walbot V. 1997. Characterization of the maize Mutator transposable element MURA transposase as a DNA-binding protein. Mol Cell Biol 17:5165–5175. [PubMed]
20. Rudenko GN, Walbot V. 2001. Expression and post-transcriptional regulation of maize transposable element MuDR and its derivatives. Plant Cell 13:553–570. [CrossRef]
21. Raizada MN, Nan GL, Walbot V. 2001. Somatic and germinal mobility of the RescueMu transposon in transgenic maize. Plant Cell 13:1587–1608. [PubMed][CrossRef]
22. Raizada MN, Benito MI, Walbot V. 2001. The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs. Plant J 25:79–91. [PubMed][CrossRef]
23. Donlin MJ, Lisch D, Freeling M. 1995. Tissue-specific accumulation of MURB, a protein encoded by MuDR, the autonomous regulator of the Mutator transposable element family. Plant Cell 7:1989–2000. [PubMed][CrossRef]
24. Hsia AP, Schnable PS. 1996. DNA sequence analyses support the role of interrupted gap repair in the origin of internal deletions of the maize transposon, MuDR. Genetics 142:603–618. [PubMed]
25. Lisch D, Freeling M. 1994. Loss of Mutator activity in a minimal line. Maydica 39:289–300.
26. Rudenko GN, Ono A, Walbot V. 2003. Initiation of silencing of maize MuDR/Mu transposable elements. Plant J 33:1013–1025. [PubMed][CrossRef]
27. Woodhouse MR, Freeling M, Lisch D. 2006. Initiation, establishment, and maintenance of heritable MuDR transposon silencing in maize are mediated by distinct factors. PLoS Biol 4:e339. [PubMed][CrossRef]
28. Strommer JN, Hake S, Bennetzen JL, Taylor WC, Freeling M. 1982. Regulatory mutants of the maize Adh1 gene caused by DNA insertions. Nature 300:542–544. [CrossRef]
29. Bennetzen JL. 1984. Transposable element Mu1 is found in multiple copies only in Robertson's Mutator maize lines. J Mol Appl Genet 2:519–524. [PubMed]
30. Taylor LP, Chandler VL, Walbot V. 1986. Insertion of 1.4 kb Mu elements into the bronze1 gene of Zea mays L. Maydica 31:31–45.
31. Taylor LP, Walbot V. 1987. Isolation and characterization of a 1.7-kb transposable element from a mutator line of maize. Genetics 117:297–307. [PubMed]
32. Oishi K, Freeling M. 1983. The Mu3 transposon in maize, p 289–292. In Nelson O (ed), Plant Transposable Elements. Plenum Press, New York, NY.
33. Talbert LE, Chandler VL. 1988. Characterization of a highly conserved sequence related to mutator transposable elements in maize. Mol Biol Evol 5:519–529. [PubMed]
34. Dietrich CR, Cui F, Packila ML, Li J, Ashlock DA, Nikolau BJ, Schnable PS. 2002. Maize Mu transposons are targeted to the 5′ untranslated region of the gl8 gene and sequences flanking Mu target-site duplications exhibit nonrandom nucleotide composition throughout the genome. Genetics 160:697–716. [PubMed]
35. Schnable P, Peterson PA. 1989. Genetic evidence of a relationship between two maize transposable element systems: Cy and Mutator. Mol Gen Genet 215:317–321. [CrossRef]
36. Fleenor D, Spell M, Robertson D, Wessler S. 1990. Nucleotide sequence of the maize Mutator element, Mu8. Nucleic Acids Res 18:6725. [PubMed][CrossRef]
37. Tan BC, Chen Z, Shen Y, Zhang Y, Lai J, Sun SS. 2011. Identification of an active new mutator transposable element in maize. G3 (Bethesda) 1:293–302. [PubMed][CrossRef]
38. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR. 2004. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573. [PubMed][CrossRef]
39. Walbot V, Britt AB, Luehrsen K, McLaughlin M, Warren C. 1988. Regulation of mutator activities in maize. Basic Life Sci 47:121–135. [PubMed]
40. Robertson DS. 1986. Genetic studies on the loss of mu mutator activity in maize. Genetics 113:765–773. [PubMed]
41. Chandler VL, Walbot V. 1986. DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A 83:1767–1771. [PubMed][CrossRef]
42. Martienssen R, Baron A. 1994. Coordinate suppression of mutations caused by Robertson's mutator transposons in maize. Genetics 136:1157–1170. [PubMed]
43. Walbot V. 1986. Inheritance of mutator activity in Zea mays as assayed by somatic instability of the bz2-mu1 allele. Genetics 114:1293–1312. [PubMed]
44. Slotkin RK. 2005. The heritable epigenetic silencing of mutator transposons by Mu killer. Ph.D. University of California at Berkeley, Berkeley, CA.
45. Skibbe DS, Fernandes JF, Medzihradszky KF, Burlingame AL, Walbot V. 2009. Mutator transposon activity reprograms the transcriptomes and proteomes of developing maize anthers. Plant J 59:622–633. [PubMed][CrossRef]
46. Schnable PS, Peterson PA. 1988. The mutator-related Cy transposable element of Zea mays L. behaves as a near-Mendelian factor. Genetics 120:587–596. [PubMed]
47. Schnable PS, Peterson PA, Saedler H. 1989. The bz-rcy allele of the Cy transposable element system of Zea mays contains a Mu-like element insertion. Mol Gen Genet 217:459–463. [PubMed][CrossRef]
48. Robertson DS, Stinard PS. 1989. Genetic analyses of putative two-element systems regulating somatic mutability in Mutator-induced aleurone mutants of maize. Dev Genet 10:482–506. [CrossRef]
49. Lisch D. 1995. Genetic and molecular characterization of the Mutator system in maize. Ph.D. University of California at Berkeley, Berkeley, CA.
50. Guerillot R, Siguier P, Gourbeyre E, Chandler M, Glaser P. 2014. The diversity of prokaryotic DDE transposases of the mutator superfamily, insertion specificity, and association with conjugation machineries. Genome Biol Evol 6:260–272. [PubMed][CrossRef]
51. Eisen JA, Benito MI, Walbot V. 1994. Sequence similarity of putative transposases links the maize Mutator autonomous element and a group of bacterial insertion sequences. Nucleic Acids Res 22:2634–2636. [PubMed][CrossRef]
52. Hua-Van A, Capy P. 2008. Analysis of the DDE motif in the Mutator superfamily. J Mol Evol 67:670–681. [PubMed][CrossRef]
53. Loessner I, Dietrich K, Dittrich D, Hacker J, Ziebuhr W. 2002. Transposase-dependent formation of circular IS256 derivatives in Staphylococcus epidermidis and Staphylococcus aureus. J Bacteriol 184:4709–4714. [PubMed][CrossRef]
54. Prudhomme M, Turlan C, Claverys JP, Chandler M. 2002. Diversity of Tn4001 transposition products: the flanking IS256 elements can form tandem dimers and IS circles. J Bacteriol 184:433–443. [PubMed][CrossRef]
55. Sundaresan V, Freeling M. 1987. An extrachromosomal form of the Mu transposons of maize. Proc Natl Acad Sci U S A 84:4924–4928. [PubMed][CrossRef]
56. Li Y, Harris L, Dooner HK. 2013. TED, an autonomous and rare maize transposon of the mutator superfamily with a high gametophytic excision frequency. Plant Cell 25:3251–3265. [PubMed][CrossRef]
57. Levy AA, Britt AB, Luehrsen KR, Chandler VL, Warren C, Walbot V. 1989. Developmental and genetic aspects of Mutator excision in maize. Dev Genet 10:520–531. [PubMed][CrossRef]
58. Levy AA, Walbot V. 1990. Regulation of the timing of transposable element excision during maize development. Science 248:1534–1537. [PubMed][CrossRef]
59. Raizada MN, Walbot V. 2000. The late developmental pattern of Mu transposon excision is conferred by a cauliflower mosaic virus 35S -driven MURA cDNA in transgenic maize. Plant Cell 12:5–21. [PubMed]
60. Yu W, Lamb JC, Han F, Birchler JA. 2007. Cytological visualization of DNA transposons and their transposition pattern in somatic cells of maize. Genetics 175:31–39. [PubMed][CrossRef]
61. Britt AB, Walbot V. 1991. Products of Mu Excision from the bronze1 gene of Zea-mays. J Cell Biochem Suppl 15:99.
62. Doseff A, Martienssen R, Sundaresan V. 1991. Somatic excision of the Mu1 transposable element of maize. Nucleic Acids Res 19:579–584. [PubMed][CrossRef]
63. Robertson DS. 1981. Mutator activity in maize: timing of its activation in ontogeny. Science 213:1515–1517. [PubMed][CrossRef]
64. Lisch D, Chomet P, Freeling M. 1995. Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics 139:1777–1796. [PubMed]
65. Fernandes J, Dong Q, Schneider B, Morrow DJ, Nan GL, Brendel V, Walbot V. 2004. Genome-wide mutagenesis of Zea mays L. using RescueMu transposons. Genome Biol 5:R82. [PubMed][CrossRef]
66. McCarty DR, Suzuki M, Hunter C, Collins J, Avigne WT, Koch KE. 2013. Genetic and molecular analyses of UniformMu transposon insertion lines. Methods Mol Biol 1057:157–166. [PubMed][CrossRef]
67. Liu S, Yeh CT, Ji T, Ying K, Wu H, Tang HM, Fu Y, Nettleton D, Schnable PS. 2009. Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet 5:e1000733. [PubMed][CrossRef]
68. Carels N, Bernardi G. 2000. Two classes of genes in plants. Genetics 154:1819–1825. [PubMed]
69. Fedoroff NV. 2013. McClintock and epigenetics. In Fedoroff NV (ed), Plant Transposons and Genome Dynamics in Evolution. Wiley-Blackwell, Oxford.
70. Martienssen R, Barkan A, Taylor WC, 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. [PubMed][CrossRef]
71. Girard L, Freeling M. 2000. Mutator-suppressible alleles of rough sheath1 and liguleless3 in maize reveal multiple mechanisms for suppression. Genetics 154:437–446. [PubMed]
72. Lowe B, Mathern J, Hake S. 1992. Active Mutator elements suppress the knotted phenotype and increase recombination at the Kn1-O tandem duplication. Genetics 132:813–822. [PubMed]
73. Greene B, Walko R, Hake S. 1994. Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics 138:1275–1285. [PubMed]
74. Cui X, Hsia AP, Liu F, Ashlock DA, Wise RP, Schnable PS. 2003. Alternative transcription initiation sites and polyadenylation sites are recruited during Mu suppression at the rf2a locus of maize. Genetics 163:685–698. [PubMed]
75. Fowler JE, Meuhlbauer GJ, Freeling M. 1996. Mosaic analysis of the liguleless3 mutant phenotype in maize by coordinate suppression of mutator-insertion alleles. Genetics 143:489–503. [PubMed]
76. Lisch D. 2013. Regulation of the Mutator system of transposons in maize. Methods Mol Biol 1057:123–142. [PubMed][CrossRef]
77. McClintock B. 1958. The suppressor-mutator system of control of gene action in maize. Carnegie Inst Wash Yr Bk 57:415–429.
78. Feschotte C, Pritham EJ. 2009. A cornucopia of Helitrons shapes the maize genome. Proc Natl Acad Sci U S A 106:19747–19748. [PubMed][CrossRef]
79. Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE. 2005. The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297. [PubMed][CrossRef]
80. Martienssen RA. 1996. Epigenetic silencing of Mu transposable elements in maize, p 593–608. In Cold Spring Harbor monograph series: epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, Plainview, NY.
81. Brown J, Sundaresan V. 1992. Genetic study of the loss and restoration of mutator transposon activity in maize - evidence against dominant-negative regulator associated with loss of activity. Genetics 130:889–898. [PubMed]
82. Slotkin RK, Freeling M, Lisch D. 2005. Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644. [PubMed][CrossRef]
83. Slotkin RK, Freeling M, Lisch D. 2003. Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays. Genetics 165:781–797. [PubMed]
84. Li H, Freeling M, Lisch D. 2010. Epigenetic reprogramming during vegetative phase change in maize. Proc Natl Acad Sci U S A 107:22184–22189. [PubMed][CrossRef]
85. Walbot V, Evans MM. 2003. Unique features of the plant life cycle and their consequences. Nat Rev Genet 4:369–379. [PubMed][CrossRef]
86. Nogueira FTS, Sarkar AK, Chitwood DH, Timmermans MCP. 2006. Organ polarity in plants is specified through the opposing activity of two distinct small regulatory RNAs. Cold Spring Harb Symp Quant Biol 71:157–164. [PubMed][CrossRef]
87. Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, Belausov E, Citovsky V, Gafni Y. 2008. Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci USA 105:157–161. [PubMed][CrossRef]
88. Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R, Watanabe Y. 2009. SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett 583:1261–1266. [PubMed][CrossRef]
89. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221. [PubMed][CrossRef]
90. Pekker I, Alvarez JP, Eshed Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910. [PubMed][CrossRef]
91. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472. [PubMed][CrossRef]
92. Creasey KM, Zhai J, Borges F, Van Ex F, Regulski M, Meyers BC, Martienssen RA. 2014. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508:411–415. [PubMed][CrossRef]
93. Borges F, Martienssen RA. 2013. Establishing epigenetic variation during genome reprogramming. RNA Biol 10:490–494. [PubMed][CrossRef]
94. Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205. [PubMed][CrossRef]
95. Gehring M, Bubb KL, Henikoff S. 2009. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324:1447–1451. [PubMed][CrossRef]
96. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, Zilberman D. 2009. Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451–1454. [PubMed][CrossRef]
97. Wollmann H, Berger F. 2012. Epigenetic reprogramming during plant reproduction and seed development. Curr Opin Plant Biol 15:63–69. [PubMed][CrossRef]
98. Mari-Ordonez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet 45:1029–1039. [PubMed][CrossRef]
99. Di Serio F, Martinez de Alba AE, Navarro B, Gisel A, Flores R. 2010. RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J Virol 84:2477–2489. [PubMed][CrossRef]
100. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–875. [PubMed][CrossRef]
101. Brosnan CA, Voinnet O. 2011. Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr Opin Plant Biol 14:580–587. [PubMed][CrossRef]
102. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL. 2006. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442:295–298. [PubMed][CrossRef]
103. Nobuta K, Lu C, Shrivastava R, Pillay M, De Paoli E, Accerbi M, Arteaga-Vazquez M, Sidorenko L, Jeong DH, Yen Y, Green PJ, Chandler VL, Meyers BC. 2008. Distinct size distribution of endogeneous siRNAs in maize: Evidence from deep sequencing in the mop1-1 mutant. Proc Natl Acad Sci U S A 105:14958–14963. [PubMed][CrossRef]
104. Woodhouse MR, Freeling M, Lisch D. 2006. The mop1 ( mediator of paramutation1) mutant progressively reactivates one of the two genes encoded by the MuDR transposon in maize. Genetics 172:579–592. [PubMed][CrossRef]
105. Singh J, Freeling M, Lisch D. 2008. A position effect on the heritability of epigenetic silencing. PLoS Genet 4:e1000216. [PubMed][CrossRef]
106. Walbot V. 1999. UV-B damage amplified by transposons in maize. Nature 397:398–399. [PubMed][CrossRef]
107. Questa JI, Walbot V, Casati P. 2010. Mutator transposon activation after UV-B involves chromatin remodeling. Epigenetics 5:352–363. [PubMed][CrossRef]
108. Qian Y, Cheng X, Liu Y, Jiang H, Zhu S, Cheng B. 2010. Reactivation of a silenced minimal Mutator transposable element system following low-energy nitrogen ion implantation in maize. Plant Cell Rep 29:1365–1376. [PubMed][CrossRef]
109. Candela H, Hake S. 2008. The art and design of genetic screens: maize. Nat Rev Genet 9:192–203. [PubMed]
110. Walbot V, Questa J. 2013. Using MuDR/Mu transposons in directed tagging strategies. Methods Mol Biol 1057:143–155. [PubMed][CrossRef]
111. Williams-Carrier R, Stiffler N, Belcher S, Kroeger T, Stern DB, Monde RA, Coalter R, Barkan A. 2010. Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J 63:167–177. [PubMed]
112. May BP, Liu H, Vollbrecht E, Senior L, Rabinowicz PD, Roh D, Pan X, Stein L, Freeling M, Alexander D, Martienssen R. 2003. Maize-targeted mutagenesis: A knockout resource for maize. Proc Natl Acad Sci U S A 100:11541–11546. [PubMed][CrossRef]
113. Settles AM, Holding DR, Tan BC, Latshaw SP, Liu J, Suzuki M, Li L, O'Brien BA, Fajardo DS, Wroclawska E, Tseung CW, Lai J, Hunter CT 3rd, Avigne WT, Baier J, Messing J, Hannah LC, Koch KE, Becraft PW, Larkins BA, McCarty DR. 2007. Sequence-indexed mutations in maize using the UniformMu transposon-tagging population. BMC Genomics 8:116. [PubMed][CrossRef]
114. Xu Z, Yan X, Maurais S, Fu H, O'Brien DG, Mottinger J, Dooner HK. 2004. Jittery, a Mutator distant relative with a paradoxical mobile behavior: excision without reinsertion. Plant Cell 16:1105–1114. [PubMed][CrossRef]
115. Feschotte C, Pritham EJ. 2007. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368. [PubMed][CrossRef]
116. Babu MM, Iyer LM, Balaji S, Aravind L. 2006. The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res 34:6505–6520. [PubMed][CrossRef]
117. Gao D. 2012. Identification of an active Mutator-like element ( MULE) in rice (Oryza sativa). Mol Genet Genomics 287:261–271. [PubMed][CrossRef]
118. Chalvet F, Grimaldi C, Kaper F, Langin T, Daboussi MJ. 2003. Hop, an active Mutator-like element in the genome of the fungus Fusarium oxysporum. Mol Biol Evol 20:1362–1375. [PubMed][CrossRef]
119. 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 15:591–602. [PubMed][CrossRef]
120. Fu Y, Kawabe A, Etcheverry M, Ito T, Toyoda A, Fujiyama A, Colot V, Tarutani Y, Kakutani T. 2013. Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J 32:2407–2417. [PubMed][CrossRef]
121. van Leeuwen H, Monfort A, Puigdomenech P. 2007. Mutator-like elements identified in melon, Arabidopsis and rice contain ULP1 protease domains. Mol Genet Genomics 277:357–364. [PubMed][CrossRef]
122. Hoen DR, Park KC, Elrouby N, Yu Z, Mohabir N, Cowan RK, Bureau TE. 2006. Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol 23:1254–1268. [PubMed][CrossRef]
123. Yu Z, Wright SI, Bureau TE. 2000. Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics 156:2019–2031. [PubMed]
124. Bao W, Kapitonov VV, Jurka J. 2010. Ginger DNA transposons in eukaryotes and their evolutionary relationships with long terminal repeat retrotransposons. Mob DNA 1:3. [PubMed][CrossRef]
125. Bao W, Jurka J. 2008. MuDr-type DNA transposons from Hydra magnipapillata. Repbase Rep 8:2075–2075.
126. Bao W, Jurka J. 2009. MuDr-type DNA transposons from Branchiostoma floridae. Repbase Rep 9:683–683.
127. Bohne A, Zhou Q, Darras A, Schmidt C, Schartl M, Galiana-Arnoux D, Volff JN. 2012. Zisupton–a novel superfamily of DNA transposable elements recently active in fish. Mol Biol Evol 29:631–645. [PubMed][CrossRef]
128. Bergink S, Jentsch S. 2009. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458:461–467. [PubMed][CrossRef]
129. Rocha EP. 2013. Evolution. With a little help from prokaryotes. Science 339:1154–1155. [PubMed][CrossRef]
130. Schaack S, Gilbert C, Feschotte C. 2010. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546. [PubMed][CrossRef]
131. Diao X, Freeling M, Lisch D. 2006. Horizontal transfer of a plant transposon. PLoS Biol 4:e5. [PubMed][CrossRef]
132. El Baidouri M, Carpentier MC, Cooke R, Gao D, Lasserre E, Llauro C, Mirouze M, Picault N, Jackson SA, Panaud O. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24:831–838. [PubMed][CrossRef]
133. Roulin A, Piegu B, Fortune PM, Sabot F, D'Hont A, Manicacci D, Panaud O. 2009. Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae. BMC Evol Biol 9:58. [PubMed][CrossRef]
134. Lisch D. 2005. Pack-MULEs: theft on a massive scale. Bioessays 27:353–355. [PubMed][CrossRef]
135. Jiang N, Ferguson AA, Slotkin RK, Lisch D. 2011. Pack-Mutator-like transposable elements ( Pack-MULEs) induce directional modification of genes through biased insertion and DNA acquisition. Proc Natl Acad Sci U S A 108:1537–1542. [PubMed][CrossRef]
136. Hanada K, Vallejo V, Nobuta K, Slotkin RK, Lisch D, Meyers BC, Shiu SH, Jiang N. 2009. The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell 21:25–38. [PubMed][CrossRef]
137. Jiang SY, Christoffels A, Ramamoorthy R, Ramachandran S. 2009. Expansion mechanisms and functional annotations of hypothetical genes in the rice genome. Plant Physiol 150:1997–2008. [PubMed][CrossRef]
138. Barkan A, Martienssen RA. 1991. Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci U S A 88:3502–3506. [CrossRef]
139. Lisch D. 2013. How important are transposons for plant evolution? Nat Rev Genet 14:49–61. [PubMed][CrossRef]
140. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405. [PubMed][CrossRef]
141. Miller WJ, McDonald JF, Pinsker W. 1997. Molecular domestication of mobile elements. Genetica 100:261–270. [PubMed][CrossRef]
142. Sinzelle L, Izsvak Z, Ivics Z. 2009. Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci 66:1073–1093. [PubMed][CrossRef]
143. Hudson ME, Lisch DR, Quail PH. 2003. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34:453–471. [PubMed][CrossRef]
144. Hudson M, Ringli C, Boylan MT, Quail PH. 1999. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev 13:2017–2027. [PubMed][CrossRef]
145. Wang H, Deng XW. 2002. Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. EMBO J 21:1339–1349. [PubMed][CrossRef]
146. Allen T, Koustenis A, Theodorou G, Somers DE, Kay SA, Whitelam GC, Devlin PF. 2006. Arabidopsis FHY3 specifically gates phytochrome signaling to the circadian clock. Plant Cell 18:2506–2516. [PubMed][CrossRef]
147. Li G, Siddiqui H, Teng Y, Lin R, Wan XY, Li J, Lau OS, Ouyang X, Dai M, Wan J, Devlin PF, Deng XW, Wang H. 2011. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat Cell Biol 13:616–622. [PubMed][CrossRef]
148. Ouyang X, Li J, Li G, Li B, Chen B, Shen H, Huang X, Mo X, Wan X, Lin R, Li S, Wang H, Deng XW. 2011. Genome-wide binding site analysis of FAR-RED ELONGATED HYPOCOTYL3 reveals its novel function in Arabidopsis development. Plant Cell 23:2514–2535. [PubMed][CrossRef]
149. Tang W, Wang W, Chen D, Ji Q, Jing Y, Wang H, Lin R. 2012. Transposase-derived proteins FHY3/FAR1 interact with PHYTOCHROME-INTERACTING FACTOR1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24:1984–2000. [PubMed][CrossRef]
150. Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H. 2007. Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305. [PubMed][CrossRef]
151. Cowan RK, Hoen DR, Schoen DJ, Bureau TE. 2005. MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol 22:2084–2089. [PubMed][CrossRef]
152. Kajihara D, de Godoy F, Hamaji TA, Blanco SR, Van Sluys MA, Rossi M. 2012. Functional characterization of sugarcane mustang domesticated transposases and comparative diversity in sugarcane, rice, maize and sorghum. Genet Mol Biol 35:632–639. [PubMed][CrossRef]
153. Joly-Lopez Z, Forczek E, Hoen DR, Juretic N, Bureau TE. 2012. A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet 8:e1002931. [PubMed][CrossRef]
154. Jiao Y, Deng XW. 2007. A genome-wide transcriptional activity survey of rice transposable element-related genes. Genome Biol 8:R28. [PubMed][CrossRef]
155. Marsch-Martinez N. 2011. A transposon-based activation tagging system for gene function discovery in Arabidopsis. Methods Mol Biol 754:67–83. [PubMed][CrossRef]
156. Hirochika H, Okamoto H, Kakutani T. 2000. Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12:357–369. [PubMed][CrossRef]
157. Bennetzen JL, Wang H. 2014. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530. [PubMed][CrossRef]
158. Woodhouse MR, Schnable JC, Pedersen BS, Lyons E, Lisch D, Subramaniam S, Freeling M. 2010. Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol 8:e1000409. [PubMed][CrossRef]
159. Franklin AE, McElver J, Sunjevaric I, Rothstein R, Bowen B, Cande WZ. 1999. Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase. Plant Cell 11(5):809–824. [PubMed][CrossRef]
160. Li J, Harper LC, Golubovskaya I, Wang CR, Weber D, Meeley RB, McElver J, Bowen B, Cande WZ, Schnable PS. 2007. Functional analysis of maize RAD51 in meiosis and double-strand break repair. Genetics 176(3):1469–1482. [PubMed][CrossRef]
161. Bennetzen JL. 1996. The Mutator transposable element system of maize. Curr Top Microbiol Immunol 204:195–229. [PubMed][CrossRef]

Article metrics loading...



The system of transposable elements (TEs) is a highly mutagenic family of transposons in maize. Because they transpose at high rates and target genic regions, these transposons can rapidly generate large numbers of new mutants, which has made the system a favored tool for both forward and reverse mutagenesis in maize. Low copy number versions of this system have also proved to be excellent models for understanding the regulation and behavior of Class II transposons in plants. Notably, the availability of a naturally occurring locus that can heritably silence autonomous elements has provided insights into the means by which otherwise active transposons are recognized and silenced. This chapter will provide a review of the biology, regulation, evolution and uses of this remarkable transposon system, with an emphasis on recent developments in our understanding of the ways in which this TE system is recognized and epigenetically silenced as well as recent evidence that -like elements (s) have had a significant impact on the evolution of plant genomes.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...



Image of FIGURE 1

Click to view


The transposon. (A) The structure of . Terminal inverted repeats (TIRs) at either end of the element are designated TIRA and TIRB. The two transcripts are indicated above and below. Exons are depicted as boxes. Introns are depicted as thin black lines. The third intron of is only infrequently spliced out. Domains identified within the MURA protein are as indicated. (B) The sequence of TIRA (top) and TIRB (bottom). The TIR sequences shows where the transposase binds and where and transcription are initiated are as shown. Note that TIRA and TIRB are identical for the first 158 nucleotides of each TIR. Differences between TIRA and TIRB are indicated by boxed residues.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view


Structural features of nonautonomous elements in maize. Black triangles represent terminal inverted repeat (TIR) sequences. Shaded boxes represent captured host sequences, with each independent sequence indicated by a number. The cognate host genes are indicated here, along with the percent identity between the captured sequence and the host gene. and : (1) GRMZM2G117007, 94% identical (unknown function). : (2) GRMZM2G015352 (unknown function), 97% identical. (3) GRMZM2G542994 (putative mago nashi, protein), 94% identical. : (4) GRMZM2G177883 (putative receptor-like protein kinase 5 precursor), 97% identical. (5) GRMZM2G037164 (unknown function), 96% identical. : (6) GRMZM2G022945 (BRCA1 C Terminus domain containing protein), 98% identical. : (7) GRMZM2G315375 (P-glycoprotein 1), 99% identical. : (8) GRMZM2G317614 (putative nucleotide binding protein), 96% identical. : (9) GRMZM2G010000 (putative heat shock protein binding protein), 90% identical. (10) GRMZM2G120085 (subtilisin-like protease precursor), 94% identical. : (11) GRMZM2G181219 (unknown function), 96% identical. (12) AC196090.3 (putative xylem serine proteinase 1 precursor), 95% identical. (13) AC234154.1 (putative phospholipase A1), 95% identical. : (14) GRMZM2G001934 (putative receptor protein kinase TMK1 precursor), 95% identical. : (15) GRMZM2G029979 (TGACG-sequence-specific DNA-binding protein TGA-2), 97% identical (16) GRMZM2G331374 (unknown function), 100% identical (17) GRMZM2G148831 (unknown function), 97% identical. (18) GRMZM2G055809 (unknown function), 95% identical. (19) GRMZM2G126413 (VQ motif family protein), 87% identical. (20) GRMZM2G081406 (putative auxin response factor), 96% identical. (21) GRMZM2G152432 (putative calmodulin), 97% identical. (22) GRMZM2G106401 (putative xylem serine proteinase 1 precursor ), 96% identical. (23) GRMZM2G116908 (unknown fuction), 96% identical.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view


Examples of somatic excision of from in the seed (A), the sheath (B) and the anthers (C). Note that in each case, reversion events are uniformly late.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view


A model explaining the differences between late somatic and germinal element transposition. (A) In all tissues, element excision produces a double-stranded gap. What is hypothesized to vary is how that gap is repaired. (B) In germinal (and early somatic) lineages the gap is repaired using the sister chromatid, which requires that excision occurs primarily after DNA synthesis. Occasional strand slippage, mediated by short stretches of sequence homology, can result in deletions within the element. (C) In contrast, during the last few rounds of cell division in somatic tissue, the double-stranded gap is repaired using nonhomologous end joining, resulting in a characteristic set of “footprints.” In each case, the excised element can insert at a new location, but in the germinal lineage, sister-chromatid-mediated repair restores an element at the original position.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5

Click to view


A striking example of a position effect on the capacity for a element to cause somatic excision of a reporter element. (A) Somatic excisions caused by (left) and (right). (B) An example of likely transposition of during somatic development, resulting in a kernel sector with an increased level of somatic excision. (C) A rare ear sector in which has undergone a duplication during development, resulting in an ear sector in which and transposed copies of segregate. (D) Southern blot analysis of more typical, single kernel duplication events. Weakly spotted, pale and heavily spotted kernels were picked from a single ear and their DNA was examined for evidence of transposition. Analysis of the weakly spotted and pale kernels show that segregation of correlates with the weak spotting phenotype. Analysis of the heavily spotted kernels shows that in each case, a new fragment, consistent with a transposition event, appeared. Note that in some cases both and a transposed copy were present, while in others, only the transposed copy is available, suggesting that these transposition events occurred prior to meiosis.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6

Click to view


. (A) The () locus. is a rearranged element, derived from the single present in the minimal line []. The rearrangement that gave rise to also caused the complet deletion of one gene and the deletion of portions of two other genes, as well as a duplication and inversion of a portion of the 5′ end of the element. Triangles represent the TIR. Boxes represent coding sequences. Transcriptional start sites for genes are as indicated. (B) The structure of the hairpin transcript derived from relative to a element. (C) The effect of on in the first generation after a plant carrying is crossed to a plant carrying . Heavily spotted kernels are those that inherit only . Weakly spotted kernels are those that carry both and . Pale kernels lack .

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7

Click to view


Maize development. (A) An illustration of the major components of an adult maize plant. Leaves are produced sequentially as the maize plant develops, with juvenile and adult leaves being distinguished by presence of epicuticular wax (a juvenile trait) and epidermal hairs (an adult trait). Transition leaves have patches of tissue with either adult or juvenile traits. Ears and tassels are only produced once adult leaves are produced. Each maize plant can be crossed as a male, or a female, or to itself. (B) A cartoon of a maize seed, showing the location of the embryo, endosperm (a terminally differentiated nutritive tissue), and the aleurone, which is the outer cell layer of the endosperm that is competent to express color. (C) A cartoon of a mature pollen grain, which contains three nuclei. The vegetative nucleus is responsible for the development of the pollen tube, and will not contribute to the next generation. Of the two sperm cells, one will fertilize the two polar nuclei to give rise to the triploid endosperm, and one of which will fertilize the egg cell to give rise to the embryo. In each part of the plant illustrated here, tissues and cells in which a relaxation of TE silencing has been observed are indicated by red asterisks.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 8

Click to view


An illustration of the diversity of in a wide variety of species. In each case, triangles represent TIRs of various lengths. Boxes represent putative coding sequences. Black boxes represent putative transposases. All models are to scale. Names marked with one asterisks indicate elements that have been shown to be mobile. Those with two asterisks have been demonstrated to be autonomous.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0032-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error