How membranes organize during seed germination: three patterns of dynamic lipid remodelling define chilling resistance and affect plastid biogenesis

Imbibitional chilling injury during germination causes agricultural losses, but this can be overcome by osmopriming. It remains unknown how membranes reorganize during germination. Herein, we comparatively profiled changes of membrane lipids during imbibition under normal and chilling temperatures in chilling-tolerant and -sensitive soybean seeds. We found three patterns of dynamic lipid remodelling during the three phases of germination. Pattern 1 involved a gradual increase in plastidic lipids during phases I and II, with an abrupt increase during phase III. This abrupt increase was associated with initiation of photosynthesis. Pattern 3 involved phosphatidic acid (PA) first decreasing, then increasing, and finally decreasing to a low level. Patterns 1 and 3 were interrupted in chilling-sensitive seeds under low temperature, which lead a block in plastid biogenesis and accumulation of harmful PA, respectively. However, they were rescued and returned to their status under normal temperature after polyethylene glycol osmopriming. We specifically inhibited phospholipase D (PLD)-mediated PA formation in chilling-sensitive seeds of soybean, cucumber, and pea, and found their germination under low temperature was significantly improved. These results indicate that membranes undergo specific and functional reorganization of lipid composition during germination and demonstrate that PLD-mediated PA causes imibibitional chilling injury. The reorganization of membrane lipids is the most important event during the imbibition of seed germination. This study finds three patterns of dynamic lipid remodelling during the germination in soybean seeds. Two patterns are interrupted in chilling-sensitive seeds under low temperature and this may result in a block in plastid biogenesis and accumulation of harmful phosphatidic acid. Osmopriming rescues the interruption and inhibition of phospholipase D-mediated phosphatidic acid increases the germination of chilling sensitive-seeds.