The LACCASE3/5/12/13 clade mediates seed coat lignin deposition and regulates imbibition and germination

The seed coat, a multi-layered protective structure containing lignin, is critical for the survival and germination of seeds. How seed coat lignin is spatiotemporally deposited and, thus, its physiological role remain poorly understood. We identified the LAC3/5/12/13 clade in Arabidopsis as seed plant-conserved and seed coat-expressed laccases responsible for synthesizing seed coat lignin. We showed in Arabidopsis that loss of LAC3/5/12/13 function drastically reduces lignin deposition in the outer integument upon seed maturation and impairs seed coat barrier function. In the lac3/5/12/13 seeds with a highly permeable coat, phase separation of the intrinsic water potential sensor FLOE1 was significantly promoted, seed water imbibition was increased, and germination was accelerated under both normal and osmotic stress conditions. These findings highlight the importance of LAC3/5/12/13-mediated lignin deposition in the seed coat in controlling embryonic development and the potential for enhancing seed performance through LACCASE genetic engineering.