Too much sugar makes plants "pregnant": maternal sucrose signals fertilization in Arabidopsis seeds
Weijie XuiD, Miryam IannacconeiD, Dennys-Marcela Gómez-PáeziD, Sandrine Choinard, Jing LüiD, Rozenn Le HiriD, Sylvie DinantiD, Lothar KalmbachiD, Regina FeiliD, John Edward LunniD, Christian MeyeriD, Enrico MagnaniiD
Abstract
Reproduction is deemed successful if it ensures the perpetuation of the species. Nonetheless, evolution has optimized reproductive efficiency across a diverse range of strategies. Animal vivipary, the process in which embryos develop inside the parents body, allows for larger offspring and better protection. This reproductive strategy relies on a fertilization signal sent to the maternal tissues to establish an embryo-supportive environment, a process known as "maternal recognition of pregnancy". Despite being a strictly animal-only term, plants independently evolved a conceptually similar strategy: the seed habit, wherein the embryo is nourished and protected by surrounding maternal tissues. We discovered that sucrose is sufficient to trigger a fertilization-independent response in the maternal tissues of Arabidopsis ovules. Upon fertilization, the release of Polycomb-mediated repression promotes the symplastic and apoplastic flow of sucrose into the seed by modulating auxin and trehalose 6-phosphate signaling. The sucrose signal is then perceived by the TARGET OF RAPAMYCIN kinase and transduced into a gibberellin response to initiate the differentiation of the seed maternal tissues. This work revealed a zygotic-maternal interplay of hormonal and sugar signaling that drives the plant "maternal recognition of fertilization", incorporating energetic cues into developmental pathways.
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