Epidermal jasmonate perception is sufficient for all aspects of jasmonate-mediated male fertility in Arabidopsis

Jasmonate (JA) signaling is essential for several environmental responses and reproductive development in many plant species. In Arabidopsis thaliana, the most obvious phenotype of JA biosynthetic and perception mutants is profound sporophytic male sterility characterized by failure of stamen filament elongation, severe delay of anther dehiscence and pollen inviability. The site of action of JA in the context of reproductive development has been discussed, but the ideas have not been tested experimentally. To this end we used targeted expression of a COI1-YFP transgene in the coi1-1 mutant background. As COI1 is an essential component of the JA co-receptor complex, the null coi1-1 mutant is male sterile due to lack of JA perception. We show that expression of COI1-YFP in the epidermis of the stamen filament and anther in coi1 mutant plants is sufficient to rescue filament elongation, anther dehiscence and pollen viability. In contrast, filament expression alone or expression in the tapetum do not restore dehiscence and pollen viability. These results demonstrate that epidermal JA perception is sufficient for anther function and pollen viability, and suggest the presence of a JA-dependent non-autonomous signal produced in the anther epidermis to synchronize both anther dehiscence and pollen maturation. Significance Statement Jasmonic acid signaling is important for male reproductive development, but the site of JA action in this context has been debated. COI1 is an essential component of the JA co-receptor complex. Here we use tissue-specific expression of COI1-YFP transgenes in the coi1-1 null allele background to demonstrate that JA perception in the anther epidermis, but not in the filament or tapetum, restores anther dehiscence and pollen viability, supporting the idea of a JA-dependent non-autonomous signal that synchronizes anther dehiscence and pollen maturation.