Photosynthesis promotes pre-protein processing and progression of chloroplast biogenesis during early plant development

Abstract Photosynthetic activity is established during chloroplast biogenesis, but whether photosynthesis itself is required for chloroplast biogenesis has not been clarified. In this study we use 680nm red light to overexcite Photosystem II and disrupt photosynthesis in two conditional mutants (var2 and abc1k1) which reversibly arrests chloroplast biogenesis. During their biogenesis, chloroplasts import most proteins associated with photosynthesis. Some of these must be transported further across the thylakoid membrane into the thylakoid lumen by the evolutionarily conserved SEC (Secretory) and TAT (Twin Arginine Translocation) pathways, energized by ATP and the trans-thylakoid proton gradient, respectively. Most luminal thylakoid proteins are synthesized in the cytoplasm with bi-partite, cleavable targeting sequences (first for the chloroplast envelope, second for the thylakoid membrane). Two-stage cleavage of these peptides is a critical step of chloroplast biogenesis. Linked to the photosynthetic defect in var2 and abc1k1 under red light, six essential proteins at the thylakoid lumen side of Photosystems I and II were incompletely cleaved and intermediate forms accumulated to high levels in the mutants. The results show that the processing of a specific module of Photosystem-associated proteins and concomitantly progression of chloroplast biogenesis depend on active photosynthesis at the earliest stages of seedling development.