Intracellular processes can be localized for efficiency or regulation. Localized translation by chloroplastic ribosomes occurs in the biogenesis of photosystem II, one of two light-driven molecular battery chargers in the photosynthetic electron transport chain. The biogenesis of both photosystems, I and II, requires the synthesis and assembly of their constituent polypeptide subunits, pigments, and cofactors. Although these biosynthetic pathways are well characterized, less is known about when and where they occur in developing chloroplasts. We used fluorescence microscopy in the unicellular alga Chlamydomonas reinhardtii to reveal spatiotemporal organization in photosystem biogenesis. We focused on translation by chloroplastic ribosomes and chlorophyll biosynthesis in two developmental contexts of active photosystem biogenesis: 1) growth of the mature chloroplast and 2) greening of a non-photosynthetic chloroplast. The results reveal that a translation zone, a known privileged location to photosystem II biogenesis, is also privileged to photosystem I biogenesis and chlorophyll biosynthesis. This discretely localized zone contrasts with the distributions of photosystems throughout the chloroplast. We also show that the photosynthesis complexes and chloroplastic ribosomes accumulate in a specific order in synchronized cellular growth suggestive of programmed differentiation. In summary, the translation zone is a hub for photosystem biogenesis in Chlamydomonas.

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