The unusual dRemp retrotransposon is abundant, highly mutagenic, and mobilized only in the second pollen mitosis of some maize lines

Significance

The frequent spontaneous mutations recovered recently in the pollen of some maize inbred lines arise mainly from the meiotic movement of retrotransposons present in few copies in the genome. This article reports that mutations in inbred line M14, identified earlier by breeders as being highly unstable, arise exclusively from the movement at the second pollen mitosis of a short retrotransposon that is present in hundreds of copies. Thus, this finding is unique because of the multicopy nature of the mutagenic retrotransposon and the specific developmental window in which it moves. It may also shed light on the possible basis for inbred genetic instability in maize.

Abstract

The frequent mutations recovered recently from the pollen of select maize lines resulted from the meiotic mobilization of specific low-copy number long-terminal repeat (LTR) retrotransposons, which differ among lines. Mutations that arise at male meiosis produce kernels with concordant mutant phenotypes in both endosperm and embryo because the two sperms that participate in double fertilization are genetically identical. Those are in a majority. However, a small minority of kernels with a mutant endosperm carry a nonconcordant normal embryo, pointing to a postmeiotic or microgametophytic origin. In this study, we have identified the basis for those nonconcordant mutations. We find that all are produced by transposition of a defective LTR retrotransposon that we have termed dRemp (defective retroelement mobile in pollen). This element has several unique properties. Unlike the mutagenic LTR retrotransposons identified previously, dRemp is present in hundreds of copies in all sequenced lines. It seems to transpose only at the second pollen mitosis because all dRemp insertion mutants are nonconcordant yet recoverable in either the endosperm or the embryo. Although it does not move in most lines, dRemp is highly mobile in the Corn Belt inbred M14, identified earlier by breeders as being highly unstable. Lastly, it can be recovered in an array of structures, ranging from solo LTRs to tandem dRemp repeats containing several internal LTRs, suggestive of extensive recombination during retrotransposition. These results shed further light on the spontaneous mutation process and on the possible basis for inbred instability in maize.