Mitochondrial respiratory-chain deficiencies lead to a severe growth delay of state-transition-deficient mutants

P. Cardol1,2, G. Finazzi2, J. Girard-Bascou2, F. Franck1, J. Alric2, and F.A. Wollman2

1Institut de Botanique, Université de Liège, Belgium; 2Institut de Biologie Physico-Chimique, Université Paris VI, France

Over the last two decades, many studies have established that the photosynthetic apparatus of plants and algae is a flexible device that responds to changes in intracellular demand for ATP and/or reducing power. Typically photosynthetic organisms may regulate the rate of linear electron flow for CO2 fixation by operating other redox pathways or by modifying the rate of excitation of their photosystems. In particular, defects of the mitochondrial respiratory-chain lead to a higher nonphotochemical plastoquinone (PQ) reduction in thylakoid membranes. Over-reduction of PQ leads in turn to a short-term adaptation known as 'state transition', which consists in the migration of Light-Harvesting Complexes II from Photosystem (PS) II to PSI, a conformation which favors cyclic over linear electron transport in the chloroplast. In the present work, we investigated the impact of the lack of the kinase responsible for 'State transitions' in Chlamydomonas, in contexts where high non-photochemical PQ reduction rate occurs. This was achieved by measuring cell growth rates, light absorption capacities, and photosynthetic activities, of double mutants bearing the Stt9 mutation (causing a loss in the STT7 kinase) and the mitochondrial dum22 mutation (causing a loss in the respiratory-chain complexes I and III). Alternatively, the mitochondrial respiration was abolished in Stt9 mutant strain by addition of respiratory inhibitors. These experiments revealed that when reducing power accumulates in the stroma following mitochondrial deficiencies, the lack of 'state transition' process is highly damageable for cell growth. We interpret this striking observation based on the smaller PSI antenna that we observed in the double mutant. We discuss experiments performed at low light and high light intensity in terms of a decrease in the efficiency of cyclic electron transport - required to improve ATP synthesis - and an increased reduction of the plastoquinone pool at steady state due to an unbalance between PSII and PSI antenna sizes. Both changes contribute to decrease the overall yield of photosynthetic energy conversion for CO2 fixation in the stt9dum22 double mutant.

e-mail address of presenting author: pierre.cardol@ulg.ac.be