Gene networks orchestrated by MeGI: a single‐factor mechanism underlying sex determination in persimmon

Summary

Separating male and female sex organs is one of the main strategies used to maintain genetic diversity within a species. However, the genetic determinants and their regulatory mechanisms have been identified in only a few species. In dioecious persimmons, the homeodomain transcription factor, Me GI , which is the target of a Y chromosome‐encoded small‐ RNA, OGI , can determine floral sexuality. The basic features of this system are conserved in the monoecious hexaploid Oriental persimmon, in which an additional epigenetic regulation of Me GI determines floral sexuality. The downstream regulatory pathways of Me GI remain uncharacterized. In this study, we examined transcriptomic data for male and female flowers from monoecious persimmon cultivars to unveil the gene networks orchestrated by Me GI . A network visualization and cistrome assessment suggested that class‐1 KNOTTED‐like homeobox ( KNOX )/ovate family protein ( OFP)/growth regulating factors ( GRF s) and short vegetative phase ( SVP) genes mediate the differences in gynoecium and androecium development between male and female flowers, respectively. The expression of these genes is directly controlled by Me GI . The gene networks also suggested that some cytokinin, auxin, and gibberellin signaling genes function cooperatively in the KNOX/ OFP/ GRF pathway during gynoecium differentiation. Meanwhile, SVP may repress PI expression in developing androecia. Overall, our results suggest that Me GI evolved the ability to promote gynoecium development and suppress androecium development by regulating KNOX/ OFP/ GRF and SVP expression levels, respectively. These insights may help to clarify the molecular mechanism underlying the production of unisexual flowers, while also elucidating the physiological background enabling a single‐factor system to establish dioecy in plants.

Significance Statement

The evolution of sex determination systems has been a major focus in plant biology for a long time, whereas the genetic determinants or molecular pathways have not been well characterized. Transcriptomic analyses on developing flowers with various persimmon accessions unveiled the gene networks orchestrated by a sex‐determining gene, Me GI , which provided the insight into physiological mechanisms not only to develop unisexual flowers, but also to enable a ‘single‐factor’ system to evolve dioecy.