Proton Gradient Regulation 5 determines reserve partitioning between starch and lipids in C. reinhardtii

Nutrient deprivation induces reserve accumulation in unicellular algae. An absence of nitrogen in the growth media results in the reorganization of the photosynthetic apparatus and triggers an increase in starch and triacylglyceride (TAG) accumulation in different algal species. Here we study the integration of photosynthetic regulatory mechanisms with carbon partitioning under N stress in C. reinhardtii. The mutant, proton gradient regulation 5 (pgr5) is impaired in photosynthetic cyclic electron flow resulting in low chloroplastic ATP/NADPH ratios. Over a time course, under both mixotrophic and phototrophic conditions, the pgr5 mutant did not accumulate starch in the first three days, but rather degraded its meagre reserves. In contrast, there was a high TAG content in the pgr5 mutant which we show, is not linked to a selective increase in autophagy in pgr5. In all strains, proteins involved in alternative electron pathways are upregulated while Photosystem II and chlorophyll are strongly degraded; pgr5 only preferentially preserved some cyt b₆f complex. Our results show that low ATP/NADPH ratios due to an absence of cyclic electron flow in pgr5 result in the mobilization of starch and strong TAG accumulation from the onset of N stress in Chlamydomonas.