GUN1-independent retrograde signaling targets the ethylene pathway to repress photomorphogenesis

When germinating in the light, Arabidopsis seedlings undergo photomorphogenic development, characterized by short hypocotyls, greening and expanded cotyledons. Stressed chloroplasts emit retrograde signals to the nucleus that induce developmental responses and repress photomorphogenesis. The nuclear targets of these retrograde signals are not yet fully known. Here, we show that lincomycin-treated seedlings (which lack developed chloroplasts) show strong phenotypic similarities to seedlings treated with ethylene (ET) precursor 1-aminocyclopropane-1-carboxylic acid (ACC), as both signals inhibit cotyledon separation in the light. We show that the lincomycin-induced phenotype partly requires a functioning ET signaling pathway, but could not detect increased ET emissions in response to lincomycin treatment. The two treatments show overlap in up-regulated gene transcripts, downstream of transcription factors ETHYLENE INSENSITIVE3 (EIN3) and EIN3-LIKE1 (EIL1). The induction of the ethylene signaling pathway is triggered by an unknown retrograde signal acting independently of GENOMES UNCOUPLED1 (GUN1). Our data show how two apparently different stress responses converge to optimize photomorphogenesis. One Sentence Summary Chloroplast retrograde signaling targets the ethylene-regulated gene network to repress photomorphogenesis in Arabidopsis