polyamine uptake transporter 2 ( put2) and decaying seeds enhance phyA-mediated germination by overcoming PIF1 repression of germination

摘要

Red light promotes germination after activating phytochrome phyB, which destabilizes the germination repressor PIF1. Early upon seed imbibition, canopy light, unfavorable for photosynthesis, represses germination by stabilizing PIF1 after inactivating phyB. Paradoxically, later upon imbibition, canopy light stimulates germination after activating phytochrome phyA. phyA-mediated germination is poorly understood and, intriguingly, is inefficient, compared to phyB-mediated germination, raising the question of its physiological significance. A genetic screen identified polyamine uptake transporter 2 ( put2 ) mutants that overaccumulate polyamines, a class of antioxidant polycations implicated in numerous cellular functions, which we found promote phyA-mediated germination. In WT seeds, our data suggest that canopy light represses polyamines accumulation through PIF1 while red light promotes polyamines accumulation. We show that canopy light also downregulates PIF1 levels, through phyA; however, PIF1 reaccumulates rapidly, which limits phyA-mediated germination. High polyamines levels in decaying seeds bypass PIF1 repression of germination and stimulate phyA-mediated germination, suggesting an adaptive mechanism promoting survival when viability is compromised. Author summary Canopy light, unfavorable for photosynthesis, elicits paradoxical responses in seeds. Depending on the timing of irradiation upon seed imbibition, canopy light can either block or promote germination. The promotion effect is mediated by the light sensor phyA and, intriguingly, it is poorly efficient when compared to that of red light, which is favorable for photosynthesis. Why would germination be stimulated by canopy light, which is not favorable for young seedling photosynthesis? We show that phyA-mediated germination is greatly enhanced in decaying seeds, which overaccumulate polyamines, a class of antioxidant molecules that promote germination. We propose an adaptive rationale for phyA-mediated germination: in decaying seeds it becomes advantageous to germinate even under canopy light as a last chance for seedling survival.