Photosynthetic organisms use sunlight as the primary source of energy to support their metabolism. In eukaryotes, reactions responsible of the conversion of light into chemical energy occur in specific organelles, the chloroplasts. In this study, we showed that mitochondria also have a seminal influence on cells' energy metabolism and on photosynthetic reactions. This is illustrated by the observation that the strong photosensitivity of Chlamydomonas reinhardtii cells depleted of the chloroplast protein PGRL1 was rescued by the introduction of a mitochondrial mutation affecting respiratory complex I. Functional analysis showed that such a reduced respiratory activity influenced chloroplast electron transport with consequent overreduction of plastoquinone and donor-side limitation of photosystem I (PSI). As a consequence, damage due to excess light affected more photosystem II (PSII) rather than PSI. Double mutant cells are able to grow under excess illumination, while single pgrl1 are not, thanks to the presence of an efficient repair mechanism of PSII. These results also underline the seminal biological relevance of the regulation of electron transport reactions within the photosynthetic complexes. Photosynthetic organisms evolved a strategy to respond to excess light where damage is targeting preferentially to a specific complex, PSII. Cells are able to endure extensive damage targeting this complex thanks to an efficient repair mechanisms, while if PSI is affected, there are drastic consequences on growth.
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