Reversibility of sex changes in the plant kingdom: more important than we thought?

Abstract

Compared to animals, plants show a wide range of reproductive strategies with different degrees of sex separation (e.g. dioecy, monoecy, hermaphroditism). While sex expression was previously thought to be genetically determined and fixed in plants, accumulating evidence suggests that sex expression can change reversibly even within one generation (sex changes), involving non-genetic factors (i.e. environment and epigenetics). In addition, recent work suggests that sex determination itself relies on epigenetic factors. Therefore, in this review, we propose that the border between sex changes and the apparently "fixed" determination of sexes is less clear than previously thought, as they rely on similar mechanisms, in particular epigenetics. Specifically, we propose that within-generation sex changes may facilitate evolutionary transitions between different degrees of sex separation via the assimilation of epimutations into genetic mutations. We then evaluate the (mal)adaptive potential of sex changes. We conclude that in the face of global environmental changes, sex changes may follow a bet-hedging evolutionary strategy, that is a heritable ability to reverse sexes. Sexual bet-hedging with an epigenetic basis (via stochastic epimutations) may help plants alleviate the deleterious consequences of climate change.