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.

Composite or closely linked maize (Zea mays) Ac/Ds transposable elements can induce chromosome breakage, but the precise configurations of Ac/Ds elements that can lead to chromosome breakage are not completely defined. Here, we determined the structures and chromosome breakage properties of 15 maize p1 alleles: each allele contains a fixed fractured Ac (fAc) element and a closely linked full-length Ac at various flanking sites. Our results show that pairs of Ac/fAc elements in which the termini of different elements are in direct or reverse orientation can induce chromosome breakage. By contrast, no chromosome breakage is observed with alleles containing pairs of Ac/fAc elements in which the external termini of the paired elements can function as a macrotransposon. Among the structures that can lead to chromosome breaks, breakage frequency is inversely correlated with the distance between the interacting Ac/Ds termini. These results provide new insight into the mechanism of transposition-induced chromosome breakage, which is one outcome of the chromosome-restructuring ability of alternative transposition events.