Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Abstract

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 (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 the long day (LD) condition, both ndufs8.1 and ndufs8.2 single mutants were indistinguishable from Columbia-0 at phenotypic and biochemical levels, whereas the ndufs8.1 ndufs8.2 double mutant was devoid of detectable holo-CI assembly/activity, showed higher alternative oxidase content/activity, and displayed a growth retardation phenotype similar to that of the ndufs4 mutant. Although growth was more affected in ndufs4 than in ndufs8.1 ndufs8.2 under the short day (SD) condition, both mutants displayed a similar impairment of growth acceleration after transfer to LD compared with the wild type. Untargeted and targeted metabolomics showed that overall metabolism was less responsive to the SD-to-LD transition in mutants than in the wild type. The typical LD acclimation of carbon and nitrogen assimilation as well as redox-related parameters was not observed in ndufs8.1 ndufs8. Similarly, NAD(H) content, which was higher in the SD condition in both mutants than in Columbia-0, did not adjust under LD. We propose that altered redox homeostasis and NAD(H) content/redox state control the phenotype of CI mutants and photoperiod acclimation in Arabidopsis.Complex I (CI; NADH:ubiquinone oxidoreductase; EC 1.6.5.3), the first enzyme of the respiratory chain of most eukaryotes, including plants, couples electron transfer to proton translocation through the inner mitochondrial membrane (Klodmann et al., 2010). CI is an L-shaped multimeric enzyme of around 1 MD in size composed of a matrix-faced peripheral arm carrying the NADH-oxidizing activity (N module), a connecting module (Q module transferring electrons to the quinonebinding site), and a hydrophobic intramembrane arm carrying the proton translocation activity (P module). Eukaryotic CI comprises more than 40 subunits, 434

Mitochondrial complex I dysfunction increases CO2 efflux and reconfigures metabolic fluxes of day respiration in tobacco leaves

“…The fact that respiratory CO 2 efflux is larger in some complex I mutants and not in others suggests that the lack of complex I activity alone is insufficient to stimulate catabolism and CO 2 efflux. Presumably, it depends on: (1) the actual reconfiguration of complex I (traces of complex I activity or the formation of subcomplexes; for a specific discussion, see Pétriacq et al ., ), (2) photorespiration; and (3) the units used to express respiration (typically the surface area or N content basis). Indeed, in the case of CMSII, which exhibited the larger respiration rate, both photorespiration (Fig.…”

“…This is typically the case in both CMSII and NMS1 mutants ( R n larger than in WT; Fig. ; Sabar et al ., ; Priault et al ., ) and in the Arabidopsis mutant ndufs8 (same R n as in WT; Pétriacq et al ., ). In addition, we found here that the increase in day respiration ( R d ) was larger than that in R n , so that the inhibition of leaf respiration by light was lower in mutants than in WT.…”

“…This effect was probably caused by the lower PEPc activity (see above) and higher consumption of aspartate to synthesize NAD, asparagine, lysine and arginine. Indeed, NAD pools have been found to be higher in complex I mutants (Dutilleul et al ., ; Kühn et al ., ; Pétriacq et al ., ). In addition, asparagine, lysine and arginine were more abundant (Table S1), whereas fumarate decreased in mutants, and was amongst the best biomarkers (Fig.…”

“…1000 kDa in size and is made up of > 40 different subunits; it comprises a large hydrophobic arm integrated to the inner membrane and a hydrophilic arm that protrudes into the matrix and contains the NADH binding site (Efremov et al ., ). Mutants lacking different complex I subunits have been described in maize (Marienfeld & Newton, ), Nicotiana sylvestris (Pla et al ., ; Gutierres et al ., ; Brangeon et al ., ), cucumber (Bartoszewski et al ., ) and Arabidopsis (Nakagawa & Sakurai, ; De Longevialle et al ., ; Meyer et al ., ; Kühn et al ., ; Pétriacq et al ., ). The best‐documented mutant is certainly cytoplasmic male sterile II (CMSII) in N. sylvestris .…”

Role of Type 2 NAD(P)H Dehydrogenase NdbC in Redox Regulation of Carbon Allocation in Synechocystis

“…In photosynthetic organisms, the NADH/NAD + status is known to regulate the coordination of nitrogen assimilation and carbon metabolism by various mechanisms (Dutilleul et al, 2005;Kämäräinen et al, 2017;Pétriacq et al, 2017). By applying a number of physiological measurements and the proteomics approach, we showed that the deletion of NdbC has a distinct effect on the metabolism of Synechocystis.…”