Chloroplast development, maintenance and function depend on the coordinated expression of chloroplast and nuclear genes. The retrograde chloroplast signals are essential in coordinating nuclear gene expression. Although the sources of signals in chloroplasts have been identified and the associated transcription factors in the nucleus extensively studied, the molecular mechanism that relays chloroplast signals to the nucleus remains a mystery. Here we show that PTm, a chloroplast envelope-bound plant homeodomain (PHD) transcription factor with transmembrane domains, functions in multiple retrograde signal pathways. The proteolytic cleavage of PTm occurs in response to retrograde signals and amino-terminal PTm accumulates in the nucleus, where it activates ABI4 transcription in a PHD-dependent manner associated with histone modifications. These results provide a molecular basis for the critical function of PTm in retrograde chloroplast signaling and shed new light on the mechanism whereby chloroplast signals are transmitted to the nucleus through the cytosol.

Seedling de-etiolation prepares plants to switch from heterotrophic to photoautotrophic growth, a transition essential for plant survival. This delicate de-etiolation process is precisely controlled by environmental and endogenous signals. Although intracellular plastid-derived retrograde signalling is essential for the de-etiolation process, the molecular nature of these retrograde signals remains elusive(1-3). Here we show that chloroplast and light signals antagonistically fine-tune a suite of developmental and physiological responses associated with de-etiolation through a transcriptional module of ABA INSENSITIVE 4 (ABI4) and ELONGATED HYPOCOTYL 5 (HY5). Moreover, ABI4 and HY5 antagonistically regulate the expression of CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and the subsequent greening process. In turn, ABI4 and HY5 are targeted for degradation by COP1 in the light and dark, respectively, to ensure a proper interplay of ABI4 and HY5 actions during seedling de-etiolation. Our study provides a new molecular mechanism for understanding how chloroplast signals converge with light signals to optimize early plant development.

Highlights d A complex of STTs acts in sorting chloroplast Tat substrates to the thylakoids d Tat substrate activates the STT complex to undergo phase separation d Hcf106 reverses phase separation and facilitates cargo translocation