Skip to main content
Genetics logoLink to Genetics
. 1999 Nov;153(3):1403–1410. doi: 10.1093/genetics/153.3.1403

Genome rearrangements by nonlinear transposons in maize.

J Zhang 1, T Peterson 1
PMCID: PMC1460832  PMID: 10545468

Abstract

Transposable elements have long been considered as potential agents of large-scale genome reorganization by virtue of their ability to induce chromosomal rearrangements such as deletions, duplications, inversions, and reciprocal translocations. Previous researchers have shown that particular configurations of transposon termini can induce chromosome rearrangements at high frequencies. Here, we have analyzed chromosomal rearrangements derived from an unstable allele of the maize P1 (pericarp color) gene. The progenitor allele contains both a full-length Ac (Activator) transposable element and an Ac terminal fragment termed fAc (fractured Ac) inserted in the second intron of the P1-rr gene. Two rearranged alleles were derived from a classical maize ear twinned sector and were found to contain a large inverted duplication and a corresponding deficiency. The sequences at the junctions of the rearrangement breakpoints indicate that the duplication and deletion structures were produced by a single transposition event involving Ac and fAc termini located on sister chromatids. Because the transposition process we describe involves transposon ends located on different DNA molecules, it is termed nonlinear transposition (NLT). NLT can rapidly break and rejoin chromosomes and thus could have played an important role in generating structural heterogeneity during genome evolution.

Full Text

The Full Text of this article is available as a PDF (275.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Athma P., Peterson T. Ac induces homologous recombination at the maize P locus. Genetics. 1991 May;128(1):163–173. doi: 10.1093/genetics/128.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennetzen J. L., Freeling M. Grasses as a single genetic system: genome composition, collinearity and compatibility. Trends Genet. 1993 Aug;9(8):259–261. doi: 10.1016/0168-9525(93)90001-x. [DOI] [PubMed] [Google Scholar]
  3. Bennetzen J. L., SanMiguel P., Chen M., Tikhonov A., Francki M., Avramova Z. Grass genomes. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):1975–1978. doi: 10.1073/pnas.95.5.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burr B., Burr F. A. Ds controlling elements of maize at the shrunken locus are large and dissimilar insertions. Cell. 1982 Jul;29(3):977–986. doi: 10.1016/0092-8674(82)90461-5. [DOI] [PubMed] [Google Scholar]
  5. Chopra S., Athma P., Li X. G., Peterson T. A maize Myb homolog is encoded by a multicopy gene complex. Mol Gen Genet. 1998 Nov;260(4):372–380. doi: 10.1007/s004380050906. [DOI] [PubMed] [Google Scholar]
  6. Chopra S., Athma P., Peterson T. Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements. Plant Cell. 1996 Jul;8(7):1149–1158. doi: 10.1105/tpc.8.7.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Courage-Tebbe U., Döring H. P., Fedoroff N., Starlinger P. The controlling element Ds at the Shrunken locus in Zea mays: structure of the unstable sh-m5933 allele and several revertants. Cell. 1983 Sep;34(2):383–393. doi: 10.1016/0092-8674(83)90372-0. [DOI] [PubMed] [Google Scholar]
  8. Dooner H. K., Belachew A. Chromosome breakage by pairs of closely linked transposable elements of the Ac-Ds family in maize. Genetics. 1991 Nov;129(3):855–862. doi: 10.1093/genetics/129.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Döring H. P., Nelsen-Salz B., Garber R., Tillmann E. Double Ds elements are involved in specific chromosome breakage. Mol Gen Genet. 1989 Oct;219(1-2):299–305. doi: 10.1007/BF00261191. [DOI] [PubMed] [Google Scholar]
  10. Döring H. P., Pahl I., Durany M. Chromosomal rearrangements caused by the aberrant transposition of double Ds elements are formed by Ds and adjacent non-Ds sequences. Mol Gen Genet. 1990 Oct;224(1):40–48. doi: 10.1007/BF00259449. [DOI] [PubMed] [Google Scholar]
  11. Emerson R A. Genetical Studies of Variegated Pericarp in Maize. Genetics. 1917 Jan;2(1):1–35. doi: 10.1093/genetics/2.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. English J. J., Harrison K., Jones JDG. Aberrant Transpositions of Maize Double Ds-Like Elements Usually Involve Ds Ends on Sister Chromatids. Plant Cell. 1995 Aug;7(8):1235–1247. doi: 10.1105/tpc.7.8.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. English J., Harrison K., Jones J. D. A genetic analysis of DNA sequence requirements for Dissociation state I activity in tobacco. Plant Cell. 1993 May;5(5):501–514. doi: 10.1105/tpc.5.5.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fedoroff N., Wessler S., Shure M. Isolation of the transposable maize controlling elements Ac and Ds. Cell. 1983 Nov;35(1):235–242. doi: 10.1016/0092-8674(83)90226-x. [DOI] [PubMed] [Google Scholar]
  15. Gray Y. H., Tanaka M. M., Sved J. A. P-element-induced recombination in Drosophila melanogaster: hybrid element insertion. Genetics. 1996 Dec;144(4):1601–1610. doi: 10.1093/genetics/144.4.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Greenblatt I. M. A chromosome replication pattern deduced from pericarp phenotypes resulting from movements of the transposable element, modulator, in maize. Genetics. 1984 Oct;108(2):471–485. doi: 10.1093/genetics/108.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Grotewold E., Drummond B. J., Bowen B., Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994 Feb 11;76(3):543–553. doi: 10.1016/0092-8674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  19. Guo M., Davis D., Birchler J. A. Dosage effects on gene expression in a maize ploidy series. Genetics. 1996 Apr;142(4):1349–1355. doi: 10.1093/genetics/142.4.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kermicle J. L. Probing the component structure of a maize gene with transposable elements. Science. 1980 Jun 27;208(4451):1457–1459. doi: 10.1126/science.208.4451.1457. [DOI] [PubMed] [Google Scholar]
  21. Kunze R. The maize transposable element activator (Ac). Curr Top Microbiol Immunol. 1996;204:161–194. doi: 10.1007/978-3-642-79795-8_8. [DOI] [PubMed] [Google Scholar]
  22. Lechelt C., Peterson T., Laird A., Chen J., Dellaporta S. L., Dennis E., Peacock W. J., Starlinger P. Isolation and molecular analysis of the maize P locus. Mol Gen Genet. 1989 Oct;219(1-2):225–234. doi: 10.1007/BF00261181. [DOI] [PubMed] [Google Scholar]
  23. Leu J. Y., Sun Y. H., Lai Y. K., Chen J. A maize cryptic Ac-homologous sequence derived from an Activator transposable element does not transpose. Mol Gen Genet. 1992 Jun;233(3):411–418. doi: 10.1007/BF00265438. [DOI] [PubMed] [Google Scholar]
  24. Lister C., Jackson D., Martin C. Transposon-induced inversion in Antirrhinum modifies nivea gene expression to give a novel flower color pattern under the control of cycloidearadialis. Plant Cell. 1993 Nov;5(11):1541–1553. doi: 10.1105/tpc.5.11.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Martin C., Lister C. Genome juggling by transposons: Tam3-induced rearrangements in Antirrhinum majus. Dev Genet. 1989;10(6):438–451. doi: 10.1002/dvg.1020100605. [DOI] [PubMed] [Google Scholar]
  26. Martínez-Férez I. M., Dooner H. K. Sesqui-Ds, the chromosome-breaking insertion at bz-m1, links double Ds to the original Ds element. Mol Gen Genet. 1997 Aug;255(6):580–586. doi: 10.1007/s004380050531. [DOI] [PubMed] [Google Scholar]
  27. McCLINTOCK B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol. 1951;16:13–47. doi: 10.1101/sqb.1951.016.01.004. [DOI] [PubMed] [Google Scholar]
  28. McClintock B. Induction of Instability at Selected Loci in Maize. Genetics. 1953 Nov;38(6):579–599. doi: 10.1093/genetics/38.6.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Peterson T. Intragenic transposition of Ac generates a new allele of the maize P gene. Genetics. 1990 Oct;126(2):469–476. doi: 10.1093/genetics/126.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Prod'hom G., Lagier B., Pelicic V., Hance A. J., Gicquel B., Guilhot C. A reliable amplification technique for the characterization of genomic DNA sequences flanking insertion sequences. FEMS Microbiol Lett. 1998 Jan 1;158(1):75–81. doi: 10.1111/j.1574-6968.1998.tb12803.x. [DOI] [PubMed] [Google Scholar]
  31. Ralston E., English J., Dooner H. K. Chromosome-breaking structure in maize involving a fractured Ac element. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9451–9455. doi: 10.1073/pnas.86.23.9451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rinehart T. A., Dean C., Weil C. F. Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis. Plant J. 1997 Dec;12(6):1419–1427. doi: 10.1046/j.1365-313x.1997.12061419.x. [DOI] [PubMed] [Google Scholar]
  33. Wang L., Kunze R. Transposase binding site methylation in the epigenetically inactivated Ac derivative Ds-cy. Plant J. 1998 Feb;13(4):577–582. doi: 10.1046/j.1365-313x.1998.00060.x. [DOI] [PubMed] [Google Scholar]
  34. Weil C. F., Wessler S. R. Molecular evidence that chromosome breakage by Ds elements is caused by aberrant transposition. Plant Cell. 1993 May;5(5):515–522. doi: 10.1105/tpc.5.5.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wirtz U., Osborne B., Baker B. Ds excision from extrachromosomal geminivirus vector DNA is coupled to vector DNA replication in maize. Plant J. 1997 Jan;11(1):125–135. doi: 10.1046/j.1365-313x.1997.11010125.x. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES