Maize Mutator transposon

Abstract

Transposable elements are widely distributed in eukaryotes. Due to its high copy numbers, high forward mutation rate and preferential insertion into low-copy DNA sequences, among others, the Mutator system has been widely used as a mutagen in genomic research. The discovery, classification, transposition specificity and epigenetic regulation of Mutator transposons were described. The application of Mutator tagging in plant genomic research was also presented. The role of Mu-like elements in genome evolution was briefly depicted. Moreover, the direction of Mutator transposon research in the future was discussed.

References

1. Aarts M G M, Dirkse W G, Stiekema W J, Pereira A (1993). Transposon tagging of a male sterility gene in Arabidopsis. Nature, 363(6431): 715–717. doi:10.1038/363715a0
2. Alleman M, Freeling M (1986). The Mu transposable elements of maize: evidencefor transposition and copy number regulation during development. Genetics, 112(1): 107–119
3. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler J E, White J, Sikkink K, Chandler V L (2006). An RNA-dependentRNA polymerase is required for paramutation in maize. Nature, 442(7100): 265–298. doi:10.1038/nature04884
4. Ambrose B A, Lerner D R, Ciceri P, Padilla C M, Yanofsky M F, Schmidt R J (2000). Molecular and genetic analyses ofthe Silky1 gene reveal conservationin floral organ specification between eudicots and monocots. Mol Cell, 5(3): 569–579. doi:10.1016/S1097-2765(00)80450-5
5. Barker R F, Thompson D V, Talbot D R, Swanson J, Bennetzen J L (1984). Nucleotidesequence of the maize transposable element Mu1. Nucleic Acids Res, 12(15): 5955–5967. doi:10.1093/nar/12.15.5955
6. Becraft P W, Freeling M (1994). Geneticanalysis of Rough sheath1 developmentalmutants of maize. Genetics, 136(1): 295–311
7. Becraft P W, Stinard P S, McCarty D R (1996). CRINKLY4: A TNFR-Like receptor kinaseinvolved in maize epidermal differentiation. Science, 273(5280): 1406–1409. doi:10.1126/science.273.5280.1406
8. Benito M I, Walbot V (1997). Characterizationof the maize Mutator transposableelement MURA transposase as a DNA-binding protein. Mol Cell Biol, 17(9): 5165–5175
9. Bennetzen J L (1996). The Mutator transposableelement system of maize. Curr Top MicrobiolImmunol, 204(1): 195–229
10. Bennetzen J L (2005). Transposable elements, gene creation and genome rearrangementin flowering plants. Curr Opin Genet Dev, 15(6): 621–627. doi:10.1016/j.gde.2005.09.010
11. Bennetzen J L, Springer P S, Cresse A D, Hendrickx M (1993). Specificity and regulation of the Mutator transposable element system in maize. Crit Rev Plant Sci, 12(1): 57–95. doi:10.1080/713608042
12. Bensen R J, Johal G S, Crane V C, Tossberg J T, Schnable P S, Meeley R B, Briggs S P (1995). Cloning and characterization of the maize An1 gene. Plant Cell, 7(1): 75–84. doi:10.1105/tpc.7.1.75
13. Blauth S L, Kim K N, Klucinec J, Shannon J C, Thompson D, Guiltinan M (2002). Identification of Mutator insertional mutants of starch-branchingenzyme 1 (sbe1) in Zea mays L. Plant Mol Biol, 48(3): 287–297. doi:10.1023/A:1013335217744
14. Blauth S L, Yao Y, Klucinec J D, Shannon J C, Thompson D B, Guilitinan M J (2001). Identification of Mutator insertional mutants of starch-branchingenzyme 2a in corn. Plant Physiol, 125(3): 1396–1405. doi:10.1104/pp.125.3.1396
15. Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005). Thick tassel dwarf1 encodes a putative maize orthologof the Arabidopsis CLAVATA1 leucine-richrepeat receptor-like kinase. Development, 132(6): 1235–1245. doi:10.1242/dev.01671
16. Brutnell T P (2002). Transposon tagging in maize. Funct Integr Genomics, 2(1): 4–12. doi:10.1007/s10142-001-0044-0
17. Brutnell T P, Sawers R J H, Mant A, Langdale J A (1999). BUNDLE SHEATH DEFECTIVE2, a novel protein required forpost-translational regulation of the rbcL gene of maize. Plant Cell, 11(5): 849–864. doi:10.1105/tpc.11.5.849
18. Buckner B, Kelson T L, Robertson D S (1990). Cloning of the y1 locus of maize, a gene involved in the biosynthesisof carotenoids. Plant Cell, 2(9): 867–876. doi:10.1105/tpc.2.9.867
19. Carey C C, Strahle J T, Selinger D A, Chandler V L (2004). Mutations in the pale aleuronecolor1 regulatory gene of the Zeamays anthocyanin pathway have distinct phenotypes relativeto the functionally similar TRANSPARENT TESTAGLABRA1 gene in Arabidopsis thaliana. Plant Cell, 16(2): 450–464. doi:10.1105/tpc.018796
20. Chalvet F, Grimaldi C, Kaper F, Langin T, Daboussi M J (2003). Hop, an active Mutator-like element in the genome of the fungus Fusarium oxysporum. Mol BiolEvol, 20(8): 1362–1375. doi:10.1093/molbev/msg155
21. Chandler V L, Walbot V (1986). DNA modificationof a maize transposable element correlates with loss of activity. Proc Natl Acad Sci USA, 83(6): 1767–1771. doi:10.1073/pnas.83.6.1767
22. Ching A, Dhugga K S, Appenzeller L, Meeley R, Bourett T M, Howard R J, Rafalski A (2006). Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchoredprotein that affects mechanical strength of maize tissues by alteringthe composition and structure of secondary cell walls. Planta, 224(5): 1174–1184. doi:10.1007/s00425-006-0299-8
23. da Costa e Silva O, Lorbiecke R, Garg P, Müller L, Waβmann M, Lauert P, Scanlon M, Hsia A P, Schnable P S, Krupinska K, Wienand U (2004). The Etched1 gene of Zeamays L. encodes a zinc ribbon protein that belongs to thetranscriptionally active chromosome (TAC) of plasmids and is similarto the transcription factor TFII S. PlantJ, 38(6): 923–939. doi:10.1111/j.1365-313X.2004.02094.x
24. Diao X M, Freeling M, Lisch D R (2006). Horizontal transfer of a plant transposon. PLoS Biol, 4(1): e5. doi: 10.1371/journal.pbio.0040005
25. Dooner H K, Weil C F (2007). Give-and-take:interactions between DNA transposons and their host plant genomes. Curr Opin Genet Dev, 17(1): 1–7. doi:10.1016/j.gde.2006.12.013
26. Edwards D, Coghill J, Batley J, Holdsworth M, Edwards K J (2002). Amplificationand detection of transposon insertion flanking sequences using fluorescent MuAFLP. Biotechniques, 32(5): 1090–1097
27. Fedoroff N V (2001). How jumping genes were discovered. Nat Struct Biol, 8(4): 300–301. doi:10.1038/86161
28. Fisk D G, Walker M B, Barkan A (1999). Molecular cloning of the maize gene crp1 reveals similarity between regulatorsof mitochondrial and chloroplast gene expression. EMBO J, 18(9): 2621–2630. doi:10.1093/emboj/18.9.2621
29. Foster T, Yamaguchi J, Wong B C, Veit B, Hake S (1999). Gnarley1 is a dominant mutation in the knox4 homeobox gene affecting cell shapeand identity. Plant Cell, 11(7): 1239–1252. doi:10.1105/tpc.11.7.1239
30. Fu S, Meeley R, Scanlon M J (2002). empty pericarp2 encodes a negative regulator of the heat shock response and is requiredfor maize embryogenesis. Plant Cell, 14(12): 3119–3132. doi:10.1105/tpc.006726
31. Gao M, Wanat J, Stinard P S, James M G, Myers A M (1998). Characterizationof dull1, a maize gene coding fora novel starch synthase. Plant Cell, 10(3): 399–412. doi:10.1105/tpc.10.3.399
32. Gray J, Close P S, Briggs S P, Johal G S (1997). A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell, 89(1): 25–31. doi:10.1016/S0092-8674(00)80179-8
33. Gupta S, Gallavotti A, Stryker G A, Schmidt R J, Lal S K (2005). A novelclass of Helitron-related transposableelements in maize contain portions of multiple pseudogenes. Plant Mol Biol, 57(1): 115–127. doi:10.1007/s11103-004-6636-z
34. Han C, Coe E H Jr, Martienssen R A (1992). Molecular cloning and characterizationof iojap (ij), a pattern striping gene of maize. EMBO J, 11(11): 4037–4046
35. Hanley S, Edwards D, Stevenson D, Haines S, Hegarty M, Schuch W, Edwards K J (2000). Identificationof transposon-tagged genes by the random sequencing of Mutator-tagged DNA fragments from Zea mays. PlantJ, 22(6): 557–566. doi:10.1046/j.1365-313x.2000.00830.x
36. Hansen J D, Pyee J, Xia Y, Wen T J, Robertson D S, Kolattukudy P E, Nikolau B J, Schnable P S (1997). The glossy1 locus of maize and an epidermis-specificcDNA from KIeinia odora definea class of receotor-like proteins required for the normal accumulationof cuticular waxes. Plant Physiol, 113(4): 1091–1100. doi:10.1104/pp.113.4.1091
37. Hardeman K J, Chandler V L (1993). Two maizegenes are each targeted predominantly by distinct classes of Mu elements. Genetics, 135(4): 1141–1150
38. Hochholdinger F, Park W J, Feix G H (2001). Cooperative action of SLR1 and SLR2 is required for lateral root-specific cell elongation in maize. Plant Physiol, 125(3): 1529–1539. doi:10.1104/pp.125.3.1529
39. Hoen D R, Park K C, Elrouby N, Yu Z H, Mohabir N, Cowan R K, Bureau T E (2006). Transposon-mediatedexpansion and diversification of a family of ULP-like genes. Mol Biol Evol, 23(6): 1254–1268. doi:10.1093/molbev/msk015
40. Hu G S, Yalpani N, Briggs S P, Johal G S (1998). A porphyrin pathway impairment is responsible for the phenotype ofa dominant disease lesion mimic mutant of maize. Plant Cell, 10(7): 1095–1105. doi:10.1105/tpc.10.7.1095
41. James M G, Robertson D S, Myers A M (1995). Characterization of the maize gene sugary1, a determinant of starch compositionin kernels. Plant Cell, 7(4): 417–429. doi:10.1105/tpc.7.4.417
42. Jane Hershberger R, Benito M I, Hardeman K J, Warren C, Chandlert V L, Walbot V (1995). Characterization of the major transcriptsencoded by the regulatory MuDR transposableelement of maize. Genetics, 140(3): 1087–1098
43. Jeddeloh J A, Bender J, Richards E J (1998). The DNA methylation locus DDM1 is required for maintenance of genesilencing in Arabidopsis. Genes Dev, 12(11): 1714–1725. doi:10.1101/gad.12.11.1714
44. Jeong D H, An S, Kang H G, Moon S, Han J J, Park S, Lee H S, An K, An G (2002). T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol, 130(4): 1636–1644. doi:10.1104/pp.014357
45. Jiang N, Bao Z R, Zhang X Y, Eddy S R, Wessler S R (2004). Pack-MULE transposableelements mediate gene evolution in plants. Nature, 431(7008): 569–573. doi:10.1038/nature02953
46. Jones D A, Thomas C M, Hammond-Kosack K E, Balint-Kurti P J, Jones J D (1994). Isolationof the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266(5186): 789–793. doi:10.1126/science.7973631
47. Juretic N, Hoen D R, Huynh M L, Harrison P M, Bureau T E (2005). The evolutionaryfate of MULE-mediated duplications of host gene fragments in rice. Genome Res, 15(9): 1292–1297. doi:10.1101/gr.4064205
48. Keith Slotkin R, Freeling M, Lisch D R (2003). Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays. Genetics, 165(2): 781–797
49. Kumar C S, Wing R A, Sundaresan V (2005). Efficient insertional mutagenesisin rice using the maize En/Spm elements. Plant J, 44(5): 879–892. doi:10.1111/j.1365-313X.2005.02570.x
50. Lai J S, Li Y B, Messing J, Dooner H K (2005). Gene movement by Helitron transposonscontributes to the haplotype variability of maize. Proc Natl Acad Sci USA, 102(25): 9068–9073. doi:10.1073/pnas.0502923102
51. Lai J S, Ma J X, Swigoňová Z, Ramakrishna W, Linton E, Llaca V, Tanyolac B, Park Y J, Jeong O Y, Bennetzen J L, Messing J (2004). Geneloss and movement in the maize genome. Genome Res, 14(10): 1924–1931. doi:10.1101/gr.2701104
52. Lisch D R (2002). Mutator transposons. Trends Plant Sci, 7(11): 498–504. doi:10.1016/S1360-1385(02)02347-6
53. Lisch D R (2005). Pack-MULEs: theft on a massive scale. Bioessays, 27(4): 353–355. doi:10.1002/bies.20219
54. Lisch D R, Carey C C, Dorweiler J E, Chandler V L (2002). A mutation that prevents paramutation in maize alsoreverses Mutator transposon methylationand silencing. Proc Natl Acad Sci USA, 99(9): 6130–6135. doi:10.1073/pnas.052152199
55. Lisch D R, Chomet P, Freeling M (1995). Genetic characterization of the Mutator system in maize: behavior and regulationof Mu transposons in a minimalline. Genetics, 139(4): 1777–1796
56. Lisch D R, Freeling M, Langham R J, Choy M Y (2001). Mutator transposase is widespreadin the grasses. Plant Physiol, 125(3): 1293–1303.. doi: 10.1104/pp.125.3.1293
57. Lisch D R, Girard L, Donlin M, Freeling M (1999). Functional analysis of deletion derivatives of the maizetransposon MuDR delineates rolesfor the MURA and MURB proteins. Genetics, 151(1): 331–341
58. Lunde C F, Morrow D J, Roy L M, Walbot V (2003). Progress in maize gene discovery: a project update. Funct Integr Genomics, 3(1): 25–32
59. Martienssen R A, Barkan A, Freeling M, Taylor W C (1989). Molecular cloning of a maize gene involved in photosynthetic membraneorganization that is regulated by Robertson's Mutator. EMBO J, 8(6): 1633–1639
60. May B P, Liu H, Vollbrecht E, Senior L, Rabinowicz P D, Roh D, Pan X K, Stein L, Freeling M, Alexander D, Martienssen R A (2003). Maize-targeted mutagenesis: a knockoutresource for maize. Proc Natl Acad SciUSA, 100(20): 11541–11546. doi:10.1073/pnas.1831119100
61. McCarty D R, Carson C B, Stinard P S, Robertson D S (1989). Molecular analysis of viviparous-1: an abscisic acid insensitive mutant of maize. Plant Cell, 1(5): 523–532. doi:10.1105/tpc.1.5.523
62. McCarty D R, Mark Settles A, Suzuki M, Tan B C, Latshaw S, Porch T, Robin K, Baier J, Avigne W, Lai J S, Messing J, Koch K E, Curtis Hannah L (2005). Steady-state transposon mutagenesisin inbred maize. Plant J, 44(1): 52–61. doi:10.1111/j.1365-313X.2005.02509.x
63. McLaughlin M, Walbot V (1987). Cloningof a mutable bz2 allele of maizeby transposon tagging and differential hybridization. Genetics, 117(4): 771–776
64. Mena M, Ambrose B A, Meeley R B, Briggs S P, Yanofsky M F, Schmidt R J (1996). Diversification of C-function activity in maize flowerdevelopment. Science, 274(5292): 1537–1540. doi:10.1126/science.274.5292.1537
65. Muehlbauer G J, Fowler J E, Girard L, Tyers R, Harper L, Freeling M (1999). Ectopic expression of the maize homeobox gene Liguleless3 alters cell fates in the leaf. Plant Physiol, 119(2): 651–662. doi:10.1104/pp.119.2.651
66. Okamoto H, Hirochika H (2001). Silencingof transposable elements in plants. TrendsPlant Sci, 6(11): 527–534. doi:10.1016/S1360-1385(01)02105-7
67. Porch T G, Tseung C W, Schmelz E A, Mark Settles A (2006). The maize Viviparous10/Viviparous13 locus encodes the Cnx1 gene required for molybdenum cofactorbiosynthesis. Plant J, 45(2): 250–263. doi:10.1111/j.1365-313X.2005.02621.x
68. Robertson D S (1978). Characterization of a Mutator system in maize. Mutat Res, 51(1): 21–28
69. Robertson D S (1980). The timing of Mu activityin maize. Genetics, 94(4): 969–978
70. Rudenko G N, Walbot V (2001). Expressionand post-transcriptional regulation of maize transposable element MuDR and its derivatives. Plant Cell, 13(3): 553–570. doi:10.1105/tpc.13.3.553
71. Ryder E, Russell S (2003). Transposableelements as tools for genomics and genetics in Drosophila. Brief Funct GenomicProteomic, 2(1): 57–71. doi:10.1093/bfgp/2.1.57
72. Scanlon M J, Myers A M (1998). Phenotypicanalysis and molecular cloning of discolored-1 (dsc1), a maize gene requiredfor early kernel development. Plant MolBiol, 37(3): 483–493. doi:10.1023/A:1005998830723
73. Schnable P S, Peterson P A (1989). Geneticevidence of a relationship between two maize transposable elementsystems: Cy and Mutator. Mol GenGenet, 215(2): 317–321. doi:10.1007/BF00339735
74. Schnable P S, Wise R P (1994). Recoveryof heritable, transposon-induced, mutant alleles of the rf2 nuclear restorer of T-cytoplasm maize. Genetics, 136(3): 1171–1185
75. Shen B, Li C, Min Z, Meeley R B, Tarczynski M C, Olsen O A (2003). sal1 determines the number of aleurone cell layers in maize endospermand encodes a class E vacuolar sorting protein. Proc Natl Acad Sci USA, 100(11): 6552–6557. doi:10.1073/pnas.0732023100
76. Singer T, Yordan C, Martienssen R A (2001). Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev, 15(5): 591–602. doi:10.1101/gad.193701
77. Smith L G, Gerttula S M, Han S, Levy J (2001). TANGLED1: a microtubule binding protein required for the spatialcontrol of cytokinesis in maize. J CellBiol, 152(1): 231–236. doi:10.1083/jcb.152.1.231
78. Stinard P S, Robertson D S, Schnable P S (1993). Genetic isolation, cloning, and analysisof a Mutator-induced, dominantantimorph of the maize amylose extender1 locus. Plant Cell, 5(11): 1555–1566. doi:10.1105/tpc.5.11.1555
79. Suzuki M, Mark Settles. A, Tseung C W, Li Q B, Latshaw S, Wu S, Porch T G, Schmelz E A, James M G, McCarty D R (2006). The maize viviparous15 locus encodes the molybdopterinsynthase small subunit. Plant J, 45(2): 264–274. doi:10.1111/j.1365-313X.2005.02620.x
80. Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D (2001). The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulatesshoot meristem proliferation in maize. Genes Dev, 15(20): 2755–2766. doi:10.1101/gad.208501
81. Talbert L E, Chandler V L (1988). Characterizationof a highly conserved sequence related to Mutator transposable elements in maize. Mol Biol Evol, 5(5): 519–529
82. Tan B C, Schwartz S H, Zeevaart J A D, McCarty D R (1997). Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA, 94(22): 12235–12240. doi:10.1073/pnas.94.22.12235
83. Timmermans M C P, Hudson A, Becraft P W, Nelson T (1999). ROUGH SHEATH2: A Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science, 284(5411): 151–153. doi:10.1126/science.284.5411.151
84. 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(4): 357–364. doi:10.1007/s00438-006-0194-9
85. Veit B, Briggs S P, Schmidt R J, Yanofsky M F, Hake S (1998). Regulationof leaf initiation by the terminal ear1 gene of maize. Nature, 393(6681): 166–168. doi:10.1038/30239
86. Walsh J, Waters C A, Freeling M (1997). The maize gene liguleless2 encodes a basic leucine zipper protein involvedin the establishment of the leaf blade-sheath boundary. Genes Dev, 11(2): 208–218
87. Winkler R G, Helentjaris T (1995). The maize Dwarf3 gene encodes a cytochrome P450-mediatedearly step in gibberellin biosynthesis. Plant Cell, 7(8): 1307–1317. doi:10.1105/tpc.7.8.1307
88. Woodhouse M R, Freeling M, Lisch D R (2006a). Initiation, establishment, and maintenanceof heritable MuDR transposon silencingin maize are mediated by distinct factors. PLoS Biol, 4(10): e339. doi: 10.1371/journal.pbio.0040339
89. Woodhouse M R, Freeling M, Lisch D R (2006b). The mop1 (mediator of paramutation1) mutantprogressively reactivates one of the two genes encoded by the MuDR transposon in maize. Genetics, 172(1): 579–592. doi:10.1534/genetics.105.051383
90. Xu X, Dietrich C R, Delledonne M, Xia Y, Wen T J, Robertson D S, Nikolau B J, Schnable P S (1997). Sequence analysis of the cloned glossy8 gene of maize suggests that it maycode for a β-ketoacyl reductase required for the biosynthesisof cuticular waxes. Plant Physiol, 115(2): 501–510. doi:10.1104/pp.115.2.501
91. Yu Z H, Wright S I, Bureau T E (2000). Mutator-like elements in Arabidopsis thaliana: structure, diversity and evolution. Genetics, 156(4): 2019–2031