Conditional modulation of NAD levels and metabolite profiles in Nicotiana sylvestris by mitochondrial electron transport and carbon/nitrogen supply

Hager, Jutta; Pellny, Till K.; Mauve, Caroline; Lelarge-Trouverie, Caroline; Paepe, Rosine De; Foyer, Christine H.; Noctor, Graham

doi:10.1007/s00425-010-1117-x

Cited by 23 publications

(22 citation statements)

References 53 publications

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“…In fact, mitochondria are known to play a key role in the nitrogen/carbon balance , which is affected in CMSII, with a marked increase in amino acids plausibly caused by high NAD(H) content (Dutilleul et al, 2005;Hager et al, 2010;Djebbar et al, 2012). Similarly, we found here that, despite lower values for parameters associated with nitrate assimilation (i.e.…”

Section: Lack Of the Ndufs8 Subunit Results In Holo-ci Misassembly Ansupporting

confidence: 79%

“…S10B), as found previously in CMSII (Hager et al, 2010). Reduction levels of pyridine nucleotides are believed to exert a control on tricarboxylic acid fluxes (Igamberdiev and Gardeström, 2003;Araújo et al, 2012), for example by controlling mitochondrial MDH activity (Tomaz et al, 2010).…”

Section: Signaling Mechanisms Possibly Involved In the Impaired Ld Acsupporting

confidence: 63%

“…This suggests that the altered photoperiod response of growth is associated with reduced levels of CI activity but not with the absence of a specific CI subunit or another genetic alteration. Previous studies in N. sylvestris (Dutilleul et al, 2003b(Dutilleul et al, , 2005Hager et al, 2010) and Arabidopsis CI mutants (Meyer et al, 2009;Keren et al, 2012;Cohen et al, 2014;Kühn et al, 2015) reported alterations in metabolic signature under standard LD conditions, with higher contents in tricarboxylic acid intermediates and amino acids. Here, we compared wild-type and mutant metabolic profiles during transfer from SD to LD by untargeted hydrophobic interaction liquid chromatography (HILIC)-quadrupole time of flight (qTOF)-mass spectrometry (MS) using leaves sampled at day 6 in the middle of the light cycle.…”

Section: Development Of Single and Double Mutants For The Ndufs8 Subumentioning

confidence: 90%

“…CMSII plants showed altered responses to environmental conditions such as light (Priault et al, 2006a), nitrogen, and CO 2 (Pellny et al, 2008;Hager et al, 2010) and were fully male sterile under very low illumination only (De Paepe et al, 1990). They were differentially affected by drought stress (Galle et al, 2010;Djebbar et al, 2012).…”

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confidence: 99%

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Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Pétriacq

Bont²,

Genestout³

et al. 2016

Plant Physiol.

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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

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Section: Lack Of the Ndufs8 Subunit Results In Holo-ci Misassembly Ansupporting

confidence: 79%

Section: Signaling Mechanisms Possibly Involved In the Impaired Ld Acsupporting

confidence: 63%

Section: Development Of Single and Double Mutants For The Ndufs8 Subumentioning

confidence: 90%

mentioning

confidence: 99%

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Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Pétriacq

Bont²,

Genestout³

et al. 2016

Plant Physiol.

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“…Metabolite determination GC-TOF-MS and HPLC analyses were as described in Hager et al (2010). In addition, free proline content was determined using the ninhydrin reaction (Magné and Larher 1992).…”

Section: Pyridine Nucleotide Determinationmentioning

confidence: 99%

Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances

Djebbar

Rzigui

Pétriacq

et al. 2011

Planta

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To investigate the role of plant mitochondria in drought tolerance, the response to water deprivation was compared between Nicotiana sylvestris wild type (WT) plants and the CMSII respiratory complex I mutant, which has low-efficient respiration and photosynthesis, high levels of amino acids and pyridine nucleotides, and increased antioxidant capacity. We show that the delayed decrease in relative water content after water withholding in CMSII, as compared to WT leaves, is due to a lower stomatal conductance. The stomatal index and the abscisic acid (ABA) content were unaffected in well-watered mutant leaves, but the ABA/stomatal conductance relation was altered during drought, indicating that specific factors interact with ABA signalling. Leaf hydraulic conductance was lower in mutant leaves when compared to WT leaves and the role of oxidative aquaporin gating in attaining a maximum stomatal conductance is discussed. In addition, differences in leaf metabolic status between the mutant and the WT might contribute to the low stomatal conductance, as reported for TCA cycle-deficient plants. After withholding watering, TCA cycle derived organic acids declined more in CMSII leaves than in the WT, and ATP content decreased only in the CMSII. Moreover, in contrast to the WT, total free amino acid levels declined whilst soluble protein content increased in CMSII leaves, suggesting an accelerated amino acid remobilisation. We propose that oxidative and metabolic disturbances resulting from remodelled respiration in the absence of Complex I activity could be involved in bringing about the lower stomatal and hydraulic conductances.

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Mitochondrial Redox State, Nitrogen Metabolism and Signalling

Foyer

2018

Annual Plant Reviews Online

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Nitrogen is often a limiting factor for plant growth and development, and therefore there is considerable interest and potential agronomic benefit not only in understanding the mechanisms that determine nitrogen use efficiency (NUE) but also in identifying new targets for NUE improvement. Much attention in recent years has focused on the core pathways and enzymes involved in primary nitrogen assimilation as well as the processes of N uptake and transport. However, recent studies on mitochondrial Complex I mutants indicate that enzymes involved in energy metabolism in the mitochondria could also be useful targets for improving NUE. TheNicotiana sylvestriscytoplasmic male sterile II (CMSII) mutant lacks respiratory Complex I, but high rates of respiration are sustained because of the presence of alternative NADH dehydrogenases. The CMSII mutation has striking effects on leaf amino acids, which are the focal point around which primary N assimilation and associated carbon metabolism and photorespiration and export occur, and on pyridine nucleotides, which are essential for metabolism and signalling. The absence of major mitochondrial NADH dehydrogenase (Complex I) in the CMSII mutant results in an N‐rich phenotype and altered N signalling. Adjustments in the abundance of Complex I relative to the alternative NADH dehydrogenases could therefore provide a mechanism for improved NUE.

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Conditional modulation of NAD levels and metabolite profiles in Nicotiana sylvestris by mitochondrial electron transport and carbon/nitrogen supply

Cited by 23 publications

References 53 publications

Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances

Mitochondrial Redox State, Nitrogen Metabolism and Signalling

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