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Photosynthesis is central to food production and the Earth's biogeochemistry, yet the molecular basis for its regulation remains poorly understood. Here, using high-throughput genetics in the model eukaryotic alga Chlamydomonas reinhardtii, we identify with high confidence (false discovery rate [FDR] < 0.11) 70 poorly characterized genes required for photosynthesis. We then enable the functional characterization of these genes by providing a resource of proteomes of mutant strains, each lacking one of these genes. The data allow assignment of 34 genes to the biogenesis or regulation of one or more specific photosynthetic complexes. Further analysis uncovers biogenesis/regulatory roles for at least seven proteins, including five photosystem I mRNA maturation factors, the chloroplast translation factor MTF1, and the master regulator PMR1, which regulates chloroplast genes via nuclear-expressed factors. Our work provides a rich resource identifying regulatory and functional genes and placing them into pathways, thereby opening the door to a system-level understanding of photosynthesis. 

Abstract Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO₂to the CO₂-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO₂-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green algaChlamydomonas reinhardtii. Our model recapitulates allChlamydomonasPCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO₂leakage, as well as proper enzyme localization to reduce futile cycling between CO₂and HCO₃⁻. Importantly, our model demonstrates the feasibility of a purely passive CO₂uptake strategy at air-level CO₂, while active HCO₃⁻uptake proves advantageous at lower CO₂levels. We propose a four-step engineering path to increase the rate of CO₂fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO₂fixed, thereby offering a framework to guide the engineering of a PCCM into land plants.