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. 1995 May;140(1):315–324. doi: 10.1093/genetics/140.1.315

Mu1-Related Transposable Elements of Maize Preferentially Insert into Low Copy Number DNA

A D Cresse 1, S H Hulbert 1, W E Brown 1, J R Lucas 1, J L Bennetzen 1
PMCID: PMC1206558  PMID: 7635296

Abstract

The Mutator transposable element system of maize was originally identified through its induction of mutations at an exceptionally high frequency and at a wide variety of loci. The Mu1 subfamily of transposable elements within this system are responsible for the majority of Mutator-induced mutations. Mu 1-related elements were isolated from active Mutator plants and their flanking DNA was characterized. Sequence analyses revealed perfect nine base target duplications directly flanking the insert for 13 of the 14 elements studied. Hybridizational studies indicated that Mu1-like elements insert primarily into regions of the maize genome that are of low copy number. This preferential selection of low copy number DNA as targets for Mu element insertion was not directed by any specific secondary structure(s) that could be detected in this study, but the 9-bp target duplications exhibited a discernibly higher than random match with the consensus sequence 5'-G-T-T-G-G/C-A-G-G/A-G-3'.

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Selected References

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  1. Alleman M., Freeling M. The Mu transposable elements of maize: evidence for transposition and copy number regulation during development. Genetics. 1986 Jan;112(1):107–119. doi: 10.1093/genetics/112.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Antequera F., Bird A. P. Unmethylated CpG islands associated with genes in higher plant DNA. EMBO J. 1988 Aug;7(8):2295–2299. doi: 10.1002/j.1460-2075.1988.tb03072.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barkan A., Martienssen R. A. 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. 1991 Apr 15;88(8):3502–3506. doi: 10.1073/pnas.88.8.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barker R. F., Thompson D. V., Talbot D. R., Swanson J., Bennetzen J. L. Nucleotide sequence of the maize transposable element Mul. Nucleic Acids Res. 1984 Aug 10;12(15):5955–5967. doi: 10.1093/nar/12.15.5955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennetzen J. L., Schrick K., Springer P. S., Brown W. E., SanMiguel P. Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome. 1994 Aug;37(4):565–576. doi: 10.1139/g94-081. [DOI] [PubMed] [Google Scholar]
  6. Bennetzen J. L., Swanson J., Taylor W. C., Freeling M. DNA insertion in the first intron of maize Adh1 affects message levels: cloning of progenitor and mutant Adh1 alleles. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4125–4128. doi: 10.1073/pnas.81.13.4125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bennetzen J. L. Transposable element Mu1 is found in multiple copies only in Robertson's Mutator maize lines. J Mol Appl Genet. 1984;2(6):519–524. [PubMed] [Google Scholar]
  8. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  9. Brown W. E., Robertson D. S., Bennetzen J. L. Molecular analysis of multiple mutator-derived alleles of the bronze locus of maize. Genetics. 1989 Jun;122(2):439–445. doi: 10.1093/genetics/122.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bureau T. E., Wessler S. R. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell. 1992 Oct;4(10):1283–1294. doi: 10.1105/tpc.4.10.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chandler V. L., Hardeman K. J. The Mu elements of Zea mays. Adv Genet. 1992;30:77–122. doi: 10.1016/s0065-2660(08)60319-3. [DOI] [PubMed] [Google Scholar]
  12. Chandler V. L., Talbert L. E., Raymond F. Sequence, genomic distribution and DNA modification of a Mu1 element from non-mutator maize stocks. Genetics. 1988 Aug;119(4):951–958. doi: 10.1093/genetics/119.4.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chandler V., Rivin C., Walbot V. Stable non-mutator stocks of maize have sequences homologous to the Mu1 transposable element. Genetics. 1986 Nov;114(3):1007–1021. doi: 10.1093/genetics/114.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chen C. H., Oishi K. K., Kloeckener-Gruissem B., Freeling M. Organ-specific expression of maize Adh1 is altered after a Mu transposon insertion. Genetics. 1987 Jul;116(3):469–477. doi: 10.1093/genetics/116.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chomet P., Lisch D., Hardeman K. J., Chandler V. L., Freeling M. Identification of a regulatory transposon that controls the Mutator transposable element system in maize. Genetics. 1991 Sep;129(1):261–270. doi: 10.1093/genetics/129.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Coen E. S., Carpenter R., Martin C. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell. 1986 Oct 24;47(2):285–296. doi: 10.1016/0092-8674(86)90451-4. [DOI] [PubMed] [Google Scholar]
  17. Cone K. C., Schmidt R. J., Burr B., Burr F. A. Advantages and limitations of using Spm as a transposon tag. Basic Life Sci. 1988;47:149–159. doi: 10.1007/978-1-4684-5550-2_11. [DOI] [PubMed] [Google Scholar]
  18. Covarrubias L., Bolivar F. Construction and characterization of new cloning vehicles. VI. Plasmid pBR329, a new derivative of pBR328 lacking the 482-base-pair inverted duplication. Gene. 1982 Jan;17(1):79–89. doi: 10.1016/0378-1119(82)90103-2. [DOI] [PubMed] [Google Scholar]
  19. Dennis E. S., Gerlach W. L., Pryor A. J., Bennetzen J. L., Inglis A., Llewellyn D., Sachs M. M., Ferl R. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 1984 May 11;12(9):3983–4000. doi: 10.1093/nar/12.9.3983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dooner H. K., Belachew A. Transposition Pattern of the Maize Element Ac from the Bz-M2(ac) Allele. Genetics. 1989 Jun;122(2):447–457. doi: 10.1093/genetics/122.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Doseff A., Martienssen R., Sundaresan V. Somatic excision of the Mu1 transposable element of maize. Nucleic Acids Res. 1991 Feb 11;19(3):579–584. doi: 10.1093/nar/19.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Döring H. P., Starlinger P. Barbara McClintock's controlling elements: now at the DNA level. Cell. 1984 Dec;39(2 Pt 1):253–259. doi: 10.1016/0092-8674(84)90002-3. [DOI] [PubMed] [Google Scholar]
  24. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  25. Greenblatt I M, Brink R A. Twin Mutations in Medium Variegated Pericarp Maize. Genetics. 1962 Apr;47(4):489–501. doi: 10.1093/genetics/47.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Greene B., Walko R., Hake S. Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics. 1994 Dec;138(4):1275–1285. doi: 10.1093/genetics/138.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hardeman K. J., Chandler V. L. Two maize genes are each targeted predominantly by distinct classes of Mu elements. Genetics. 1993 Dec;135(4):1141–1150. doi: 10.1093/genetics/135.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  29. Hulbert S. H., Richter T. E., Axtell J. D., Bennetzen J. L. Genetic mapping and characterization of sorghum and related crops by means of maize DNA probes. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4251–4255. doi: 10.1073/pnas.87.11.4251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jin Y. K., Bennetzen J. L. Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell. 1994 Aug;6(8):1177–1186. doi: 10.1105/tpc.6.8.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lee L., Fenoll C., Bennetzen J. L. Construction and Homologous Expression of a Maize Adh1 Based NcoI Cassette Vector. Plant Physiol. 1987 Oct;85(2):327–330. doi: 10.1104/pp.85.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Levy A. A., Walbot V. Molecular analysis of the loss of somatic instability in the bz2::mu1 allele of maize. Mol Gen Genet. 1991 Sep;229(1):147–151. doi: 10.1007/BF00264223. [DOI] [PubMed] [Google Scholar]
  33. Nacken W. K., Piotrowiak R., Saedler H., Sommer H. The transposable element Tam1 from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol Gen Genet. 1991 Aug;228(1-2):201–208. doi: 10.1007/BF00282466. [DOI] [PubMed] [Google Scholar]
  34. Nash J., Luehrsen K. R., Walbot V. Bronze-2 gene of maize: reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell. 1990 Nov;2(11):1039–1049. doi: 10.1105/tpc.2.11.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ortiz D. F., Rowland L. J., Gregerson R. G., Strommer J. N. Insertion of Mu into the Shrunken 1 gene of maize affects transcriptional and post-transcriptional regulation of Sh1 RNA. Mol Gen Genet. 1988 Sep;214(1):135–141. doi: 10.1007/BF00340191. [DOI] [PubMed] [Google Scholar]
  36. Sachs M. M., Dennis E. S., Gerlach W. L., Peacock W. J. Two Alleles of Maize ALCOHOL DEHYDROGENASE 1 Have 3' Structural and Poly(a) Addition Polymorphisms. Genetics. 1986 Jun;113(2):449–467. doi: 10.1093/genetics/113.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schnable P. S., Peterson P. A., Saedler H. The bz-rcy allele of the Cy transposable element system of Zea mays contains a Mu-like element insertion. Mol Gen Genet. 1989 Jun;217(2-3):459–463. doi: 10.1007/BF02464917. [DOI] [PubMed] [Google Scholar]
  38. Schwartz D. Pattern of ac transposition in maize. Genetics. 1989 Jan;121(1):125–128. doi: 10.1093/genetics/121.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  40. Springer P. S., Edwards K. J., Bennetzen J. L. DNA class organization on maize Adh1 yeast artificial chromosomes. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):863–867. doi: 10.1073/pnas.91.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Talbert L. E., Patterson G. I., Chandler V. L. Mu transposable elements are structurally diverse and distributed throughout the genus Zea. J Mol Evol. 1989 Jul;29(1):28–39. doi: 10.1007/BF02106179. [DOI] [PubMed] [Google Scholar]
  42. Taylor L. P., Walbot V. A deletion adjacent to the maize transposable element Mu-1 accompanies loss of Adh1 expression. EMBO J. 1985 Apr;4(4):869–876. doi: 10.1002/j.1460-2075.1985.tb03712.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taylor L. P., Walbot V. Isolation and characterization of a 1.7-kb transposable element from a mutator line of maize. Genetics. 1987 Oct;117(2):297–307. doi: 10.1093/genetics/117.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Van Schaik N W, Brink R A. Transpositions of Modulator, a Component of the Variegated Pericarp Allele in Maize. Genetics. 1959 Jul;44(4):725–738. doi: 10.1093/genetics/44.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Walbot V. The Mutator transposable element family of maize. Genet Eng (N Y) 1991;13:1–37. doi: 10.1007/978-1-4615-3760-1_1. [DOI] [PubMed] [Google Scholar]
  46. Walbot V., Warren C. DNA methylation in the Alcohol dehydrogenase-1 gene of maize. Plant Mol Biol. 1990 Jul;15(1):121–125. doi: 10.1007/BF00017729. [DOI] [PubMed] [Google Scholar]
  47. Zhao Z. Y., Sundaresan V. Binding sites for maize nuclear proteins in the terminal inverted repeats of the Mu1 transposable element. Mol Gen Genet. 1991 Sep;229(1):17–26. doi: 10.1007/BF00264208. [DOI] [PubMed] [Google Scholar]

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