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Epigenetic Regulation of the Maize Spm Transposable Element

Nina Fedoroff


Maize transposons, the mobile genes discovered by Barbara McClintock half a century ago, were the first plant genes known to be epigenetically silenced. Early in the study of the Suppressor-mutator (Spm) transposable element, McClintock recognized that the transposable element could be silenced heritably but not irreversibly, an odd and important observation (McClintock 1957McClintock 1958). A silent Spm transposon showed none of its usual genetic activities. It could neither itself move or cause another transposable element to move, nor could it change the expression of genes with Spm insertions, as could an active transposable element (McClintock 1956). However, a silent transposable element was different from a mutant transposable element because it could return to a genetically active form, reacquiring all of its activities simultaneously. McClintock explored the ability of the Spm element to alternate between active and silent phases in considerable genetic detail over the subsequent decade, noting that an unrelated transposon, the Activator (Ac) element, could be similarly silenced (McClintock 1959McClintock 1961McClintock 1962McClintock 1964McClintock 1965a,b, 1971). McClintock’s most striking deduction was that an active Spm could reactivate an inactive one (McClintock 1971).

We now know that both transcription and transposition of the Spm element are subject to negative epigenetic control by a molecular mechanism that involves methylation of transposable element regulatory sequences (Fedoroff 1994). The transposable element itself encodes an autoregulatory protein that promotes the reactivation of an epigenetically silenced transposable element. I review the early genetic clues in McClintock’s work pointing to the existence of both epigenetic and autoregulatory...

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