Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Plant mutants for genes encoding subunits of mitochondrial Complex I (CI, NADH:ubiquinone oxidoreductase), the first enzyme of the respiratory chain, display various phenotypes depending on growth conditions. Here, we examined the impact of photoperiod, a major environmental factor controlling plant development, on two Arabidopsis thaliana CI mutants: a new insertion mutant interrupted in both ndufs8.1 and ndufs8.2 genes encoding the NDUFS8 subunit, and the previously characterized ndufs4 CI mutant. In long day (LD) condition, both ndufs8.1 and ndufs8.2 single mutants were indistinguishable from Col-0 at phenotypic and biochemical levels, whereas the ndufs8.1 ndufs8.2 double mutant was devoid of detectable holo-CI assembly/activity, showed higher AOX content/activity and displayed a growth-retardation phenotype similar to that of the ndufs4 mutant. Although growth was more affected in ndufs4 than ndufs8.1 ndufs8.2 under short day (SD) condition, both mutants displayed a similar impairment of growth acceleration after transfer to LD as compared to the WT. Untargeted and targeted metabolomics showed that overall metabolism was less responsive to the SD-to-LD transition in mutants than in the WT. The typical LD acclimation of carbon, nitrogen-assimilation and redox-related parameters was not observed in ndufs8.1 ndufs8. Similarly, NAD(H) content, that was higher in SD condition in both mutants than in Col-0, did not adjust under LD. We propose that altered redox homeostasis and NAD(H) content/redox state control the phenotype of Complex I mutants and photoperiod acclimation in Arabidopsis.