Stigmatic papilla cells secrete jasmonic acid to promote pollen germination through calcium signaling

Double fertilization begins with signal communication between pollen grains and the pistil stigma, a process that includes pollen adhesion, hydration, germination, and penetration. While several molecular regulators governing pollen hydration and penetration have been characterized, the molecules that mediate pollen germination on the stigma remain largely unelucidated. In this study, we identified jasmonic acid (JA), a maternal factor secreted by stigmatic papilla cells, which facilitates pollen germination by elevating cytosolic Ca²⁺ levels in pollen grains. We found that pollen grains exhibited significantly slower germination in vitro than on stigmas, and that exogenous JA supplementation rescued this in vitro germination defect. We further showed that stigmatic papilla cells accumulated high concentrations of JA, which was secreted to promote pollen germination. Disruption of essential genes for JA synthesis, rather than the JA receptor COI1 in the stigma, causes defective pollen germination. JA triggers calcium elevation in pollen grains, and this elevated calcium signal is required for pollen germination and can be suppressed by calcium channel inhibitors. We found that Annexin 1 and Annexin 2, two calcium channels expressed in pollen grains, contribute to JA-triggered calcium increase in pollen grains. Consistently, applying JA on the stigma could promote interspecific pollen germination. In summary, our work identifies a new role for stigma-derived JA in promoting pollen germination by triggering calcium signaling in pollen grains.