Functional relationship between mTERF4 and GUN1 in retrograde signaling

Plastid-to-nucleus retrograde signaling plays an important role in regulating the expression of photosynthesis-associated nuclear genes (PhANGs) in accordance with physiological demands on chloroplast biogenesis and function. Despite its fundamental importance, little is known about the molecular nature of the plastid gene expression (PGE)-dependent type of retrograde signaling. PGE is a multifaceted process, and several factors, including pentatricopeptide repeat (PPR) proteins, are involved in its regulation. The PPR protein GUN1 plays a central role in PGE-dependent retrograde signaling. In this study, we isolated a mutant exhibiting up-regulation of CHLOROPHYLL A/B-BINDING PROTEIN (CAB) under normal growth conditions (named coe1 for CAB overexpression 1). The coe1 mutant has a single-base mutation in the gene for mitochondrial transcription termination factor 4 (mTERF4)/BSM/RUG2, which plays a role in regulating the processing of certain plastid transcripts. Defects in GUN1 or mTERF4 de-repressed the expression of specific plastid mRNAs in the presence of lincomycin (LIN). In wild-type plants, treatment with LIN or spectinomycin (SPE) inhibited processing of plastid transcripts. Comparative analysis revealed that in gun1 and coe1/mterf4, but not in wild-type, gun4, or gun5 plants, the processing of plastid transcripts and expression levels of Lhcb1 mRNA were affected in opposite ways when plants were grown in the presence of LIN or SPE. In addition, the coe1 mutation affected the intracellular accumulation and distribution of GUN1, as well as its plastid signaling activity. Taken together, these results suggest that GUN1 and COE1 cooperate in PGE and retrograde signaling.