State transitions correspond to a major regulation process for photosynthesis, whereby chlorophyll protein complexes responsible for light harvesting migrate between photosystem II and photosystem I in response to changes in the redox poise of the intersystem electron carriers. Here we disclose their physiological significance in Chlamydomonas reinhardtii using a genetic approach. Using single and double mutants defective for state transitions and/or mitochondrial respiration, we show that photosynthetic growth, and therefore biomass production, critically depends on state transitions in respiratory-defective conditions. When extra ATP cannot be provided by respiration, enhanced photosystem I turnover elicited by transition to state 2 is required for photosynthetic activity. Concomitant impairment of state transitions and respiration decreases the overall yield of photosynthesis, ultimately leading to reduced fitness. We thus provide experimental evidence that the combined energetic contributions of state transitions and respiration are required for efficient carbon assimilation in this alga.cyclic electron flow ͉ photosynthesis ͉ energetic metabolism S tate transitions (ST) are a short-term photosynthetic acclimation process that controls the reversible association of the photosystem II (PSII) antenna protein complex (LHCII) with either PSII (in state 1) or photosystem I (PSI) (in state 2) (1-3). This process relies on the reversible LHCII phosphorylation involving the membrane-bound protein kinase Stt7-STN7, which recently has been identified in Chlamydomonas reinhardtii and Arabidopsis thaliana (4, 5). Phosphorylation changes lead to the migration of a fraction of the antenna between the PSII-enriched membrane domains and the PSI-enriched membrane domains within the thylakoids in plant and algal chloroplasts (3, 6).STs first were observed in unicellular green algae and originally were described as a mechanism linking the redox poise of the intersystem electron carriers to changes in the absorption capacity of the photosystems (3). Reduction of the plastoquinone (PQ) pool upon increased PSII sensitization activates the kinase via the cytochrome b 6 f complex (7). Conversely, upon increased PSI sensitization, PQH 2 oxidation inactivates the kinase. P i -LHCII then is dephosphorylated by a phosphatase (3) whose biochemical nature and regulation remain elusive.In plants, STs are of limited amplitude, involving Ϸ20% of LHCII (8). Their occurrence probably is not essential for plant survival, as suggested by the very limited effects on growth (4, 9-11) and on fitness (12) of mutations preventing STs in Arabidopsis. One of these mutants shows a marked phenotype only under a very particular regimen of fluctuating light (4). In Chlamydomonas, STs involve a larger fraction of PSII antenna than in plants, with Ϸ80% of PSII antennae being involved in this phenomenon (13), including monomeric LHCII (14). The very large redistribution of light-harvesting complexes with STs in this alga is difficult to reconcile with a role...