Ethylene produced in carpel primordia controls CmHB40 expression to inhibit stamen development.

Sex determination evolved to control the development of unisexual flowers. In agriculture, it conditions how plants are cultivated and bred. We investigated how female flowers develop in monoecious cucurbits. We discovered in melon, Cucumis melo, a mechanism in which ethylene produced in the carpel is perceived in the stamen primordia through spatially differentially expressed ethylene receptors. Subsequently, the CmEIN3/CmEIL1 ethylene signalling module, in stamen primordia, activates the expression of CmHB40, a transcription factor that downregulates genes required for stamen development and upregulates genes associated with organ senescence. Investigation of melon genetic biodiversity revealed a haplotype, originating in Africa, altered in EIN3/EIL1 binding to CmHB40 promoter and associated with bisexual flower development. In contrast to other bisexual mutants in cucurbits, CmHB40 mutations do not alter fruit shape. By disentangling fruit shape and sex-determination pathways, our work opens up new avenues in plant breeding.

The gynoecious CmWIP1 transcription factor interacts with CmbZIP48 to inhibit carpel development.

In angiosperms, sex determination leads to development of unisexual flowers. In Cucumis melo, development of unisexual male flowers results from the expression of the sex determination gene, CmWIP1, in carpel primordia. To bring new insight on the molecular mechanisms through which CmWIP1 leads to carpel abortion in male flowers, we used the yeast two-hybrid approach to look for CmWIP1-interacting proteins. We found that CmWIP1 physically interacts with an S2 bZIP transcription factor, CmbZIP48. We further determined the region mediating the interaction and showed that it involves the N-terminal part of CmWIP1. Using laser capture microdissection coupled with quantitative real-time gene expression analysis, we demonstrated that CmWIP1 and CmbZIP48 share a similar spatiotemporal expression pattern, providing the plant organ context for the CmWIP1-CmbZIP48 protein interaction. Using sex transition mutants, we demonstrated that the expression of the male promoting gene CmWIP1 correlates with the expression of CmbZIP48. Altogether, our data support a model in which the coexpression and the physical interaction of CmWIP1 and CmbZIP48 trigger carpel primordia abortion, leading to the development of unisexual male flowers.