Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize

Abstract

Barbara McClintock reported that the Ac/Ds transposable element system can generate major chromosomal rearrangements (MCRs), but the underlying mechanism has not been determined. Here, we identified a series of chromosome rearrangements derived from maize lines containing pairs of closely linked Ac transposable element termini. Molecular and cytogenetic analyses showed that the MCRs in these lines comprised 17 reciprocal translocations and two large inversions. The breakpoints of all 19 MCRs are delineated by Ac termini and characteristic 8-base-pair target site duplications, indicating that the MCRs were generated by precise transposition reactions involving the Ac termini of two closely linked elements. This alternative transposition mechanism may have contributed to chromosome evolution and may also occur during V(D)J recombination resulting in oncogenic translocations.[Keywords: V(D)J recombination; chromosome rearrangements; hAT elements; transposition] Supplemental material is available at http://www.genesdev.org.

Genome Rearrangements in Maize Induced by Alternative Transposition of ReversedAc/DsTermini

“…Inversion and deletion are the major products of reversed-ends transposition: The P1-rr11 and P1-rr910 alleles condition predominantly red kernel pericarp (Zhang and Peterson 2004;Zhang et al 2009). Both alleles contain an identical fAc element in the second intron of the p1 gene and a full-length Ac element inserted upsteam of the p1 transcription start site.…”

“…The maize alleles P1-rr11, P1-rr910, and P1-ovov454 were isolated and described previously (Zhang and Peterson 2004;Zhang et al 2009;Yu et al 2010). Plants in which the P1-rr11, P1-rr910, or P1-ovov454 alleles were heterozygous with an allele for colorless kernel pericarp (p1-ww or p1-wr) were crossed by pollen from plants of genotype p1, r1-m3::Ds.…”

“…The 59 end of Ac and the 39 end of fAc are in reversed orientation, separated by a 13-kb intertransposon segment (ITS). In this configuration, reversed-ends transposition can induce a variety of chromosome rearrangements, including deletions, inversions, translocations, and ITS rearrangements (Zhang and Peterson 2004;Zhang et al 2009). In addition, this reversed-ends configuration can induce chromosome breakage (Huang and Dooner 2008;Yu et al 2010).…”

“…In contrast, most DNA elements move by a "cut and paste" mechanism. Although DNA elements are less abundant compared with retroelements, they can lead to a variety of genome structural changes (Ross et al 1979;Gray 2000;Watanabe et al 2007;Huang and Dooner 2008) including large chromosomal rearrangements, which may contribute to genome evolution (McClintock 1951;McClintock 1978;Lister et al 1993;Zhang et al 2009). …”

Structural and Functional Divergence of a 1-Mb Duplicated Region in the Soybean (Glycine max) Genome and Comparison to an Orthologous Region fromPhaseolus vulgaris

“…More structural changes (deletions) were found in the two Gm15 intervals, where there was higher transposon density, suggesting a correlation between structural changes and transposable elements. It is known that transposons can induce major genome rearrangements, including deletions, duplications, inversions, macrotransposition, and reciprocal translocations (Gray, 2000;Caceres et al, 2001;Lonnig and Saedler, 2002;Huang and Dooner, 2008;Lee et al, 2008;Zhang et al, 2009). We hypothesize that Gm15, with a higher transposon density, underwent more extensive structural changes (i.e., higher density of LTR retrotransposon, solo LTRs, and lower gene retention rate) and that transposable elements were likely an active force in this remodeling of a homoeologous chromosome in soybean (see Supplemental Figure 17 online).…”