AUTHOR=LaRue Nicole C., Sullivan Alessandra M., Di Stilio Verónica S.

TITLE=Functional recapitulation of transitions in sexual systems by homeosis during the evolution of dioecy in Thalictrum

JOURNAL=Frontiers in Plant Science

VOLUME=4

YEAR=2013

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2013.00487

DOI=10.3389/fpls.2013.00487

ISSN=1664-462X

ABSTRACT=<p>Sexual systems are highly variable in flowering plants and an important contributor to floral diversity. The ranunculid genus <italic>Thalictrum</italic> is especially well-suited to study evolutionary transitions in sexual systems. Homeotic transformation of sexual organs (stamens and carpels) is a plausible mechanism for the transition from hermaphroditic to unisexual flowers in this lineage because flowers of dioecious species develop unisexually from inception. The single-copy gene <italic>PISTILLATA</italic> (<italic>PI</italic>) constitutes a likely candidate for rapid switches between stamen and carpel identity. Here, we first characterized the expression pattern of all B class genes in the dioecious species <italic>T. dioicum</italic>. As expected, all B class orthologs are expressed in stamens from the earliest stages. Certain <italic>AP3</italic> lineages were also expressed late in sepal development. We then tested whether orthologs of <italic>PI</italic> could potentially control sexual system transitions in <italic>Thalictrum</italic>, by knocking-down their expression in <italic>T. dioicum</italic> and the hermaphroditic species <italic>T. thalictroides</italic>. In <italic>T. dioicum</italic>, we found that <italic>ThdPI-1/2</italic> silencing caused stamen primordia to develop into carpels, resulting in male to female flower conversions. In <italic>T. thalictroides</italic>, we found that <italic>ThtPI</italic> silencing caused stamen primordia to develop into supernumerary carpels, resulting in hermaphroditic to female flower conversions. These phenotypes illustrate the ability for homeotic mutations to bring about sudden and potentially adaptive changes by altering the function of a single gene. We propose a two-step evolutionary model where transitions from hermaphroditic to unisexual plants in <italic>Thalictrum</italic> result from two independent mutations at a B class gene locus. Our <italic>PI</italic> knockdown experiments in <italic>T. thalictroides</italic> recapitulate the second step in this model: the evolution of female plants as a result of a loss-of-function mutation in a B class gene.</p>