EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings

The ability to switch from skotomorphogenesis to photomorphogenesis is essential for seedling development and plant survival. Recent studies revealed that COP1 and phytochrome-interacting factors (PIFs) are key regulators of this transition by repressing the photomorphogenic responses and/or maintaining the skotomorphogenic state of etiolated seedlings. Here we report that the plant hormone ethylene plays a crucial role in the transition from skotomorphogenesis to photomorphogenesis by facilitating greening of etiolated seedlings upon light irradiation. Activation of EIN3/EIL1 is both necessary and sufficient for ethylene-induced enhancement of seedling greening, as well as repression of the accumulation of protochlorophyllide, a phototoxic intermediate of chlorophyll synthesis. EIN3/EIL1 were found to induce gene expression of two key enzymes in the chlorophyll synthesis pathway, protochlorophyllide oxidoreductase A and B (PORA/B). ChIP and EMSA assays demonstrated that EIN3 directly binds to the specific elements present in the PORA and PORB promoters. Genetic studies revealed that EIN3/EIL1 function in cooperation with PIF1 in preventing photo-oxidative damage and promoting cotyledon greening. Moreover, activation of EIN3 reverses the blockage of greening triggered by cop1 mutation or far-red light irradiation. Consistently, EIN3 acts downstream of COP1 and its protein accumulation is enhanced by COP1 but decreased by light. Taken together, EIN3/EIL1 represent a new class of transcriptional regulators along with PIF1 to optimize de-etiolation of Arabidopsis seedlings. Our study highlights the essential role of ethylene in enhancing seedling development and survival through protecting etiolated seedlings against photo-oxidative damage.