Interacting with GUN1 and MORF2, SL1 modulates plastid RNA editing during norflurazon-induced retrograde signaling.

Abstract

Chloroplast-to-nucleus retrograde signaling and plastid RNA editing are both essential for chloroplast biogenesis and plant development, but the underlying mechanism linking these two processes remains unclear. Here, we identify the mitochondrial transcription termination factor mTERF3/Seedling Lethal 1 (SL1), previously characterized as a plastid-encoded RNA polymerase (PEP)-associated protein, as a key regulator connecting RNA editing to retrograde signaling. SL1 directly interacts with GUN1 and MORF2 and is indispensable for 31 out of 34 plastid RNA editing sites in Arabidopsis. Loss of SL1 function results in a strong genome uncoupled (gun) molecular phenotype under norflurazon (NF) treatment, accompanied by defective RNA editing and complete loss of the NDH complex. Mechanistically, SL1 assembles the editosome by recruiting canonical and atypical PPR-DYW proteins (CRR28, RARE1, DYW1, and DYW2) together with multiple non-PPR editing factors, while its strong affinity to MORF2 ensures appropriate editosome stoichiometry. SL1 also colocalizes with the PEP complex, suggesting a physical coupling between transcription and RNA editing in plastid nucleoids. Furthermore, SL1 modulates RNA editing profiles and regulates GLK1/2 expression during NF-induced retrograde signaling. Our findings expand the functional repertoire of mTERF proteins and uncover a molecular mechanism that connects RNA editing with retrograde signaling through SL1.