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

Abstract

SummarySeparating 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, MeGI, 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 MeGI determines floral sexuality. The downstream regulatory pathways of MeGI 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 MeGI. A network visualization and cistrome assessment suggested that class‐1 KNOTTED‐like homeobox (KNOX)/ovate family protein (OFP)/growth regulating factors (GRFs) 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 MeGI. 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 MeGI 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.

The persimmon genome reveals clues to the evolution of a lineage-specific sex determination system in plants

“…Our evolutionary analyses revealed that the positive selection that affected MeGI specifically did not occur on the region binding to the target cis-motifs, called homeobox-domain (HB) ( Fig 4D and 4E), but rather on the 5' undefined region and on the leucine zipper region putatively forming heterodimers [26,27]. This was supported by the results of DNA affinity purification sequencing (DAP-Seq) [28] using MeGI [25] or SiMeGI fused to a Halo-tag. This allowed us to identify which genes and/or motifs is preferentially targeted by each of these transcription factors.…”

“…Table). The function of MeGI as repressor of androecium in persimmon is due to the ability to regulate PISTILLATA (PI) in young developing androecium [25]. The expression level of PI in N. tabacum was significantly down-regulated in the transgenic lines with MeGI, while the lines transformed with SiMeGI showed no changes in PI expression ( Fig 5I and 5J).…”

“…The DAP-Seq reads were mapped to the D. lotus genome to characterize the accumulated recognition motifs (see Materials and Methods). We identified the motifs using the top 1,000 high-confidence peaks, and determined that the AATWATT sequence was enriched when using MeGI [25] and SiMeGI as the probes (Fig 5K). This motif is commonly recognized by the Arabidopsis HD-ZIP1 genes as well [25,29].…”

“…We identified the motifs using the top 1,000 high-confidence peaks, and determined that the AATWATT sequence was enriched when using MeGI [25] and SiMeGI as the probes (Fig 5K). This motif is commonly recognized by the Arabidopsis HD-ZIP1 genes as well [25,29]. Thus, it is possible that the feminization role of MeGI could have resulted from either increased efficiency or novel affinity to interact with other factors.…”

Developmental basis for flower sex determination and effects of cytokinin on sex determination in Plukenetia volubilis (Euphorbiaceae)

“…The mechanisms of sex determination have been investigated in some plants, such as maize, cucumber, kiwifruit, and persimmon, which are mainly affected by genetics, plant hormones, and environmental factors (Grant et al 1994;Juarez and Banks 1998;Tanurdzic and Banks 2004;Adam et al 2011;Bai and Xu 2013;Golenberg and West 2013;Li and Communicated by Dolf Weijers. Liu 2017;Henry et al 2018;Akagi et al 2018Akagi et al , 2019Yang et al 2019).…”