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

Abstract

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.

Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

“…S3D), suggesting that photosynthetic ATP might compensate for lower mitochondrial ATP production. Nevertheless, as reported previously for CMSII (Szal et al, 2008;Djebbar et al, 2012) and ndufs4 (Meyer et al, 2009), total leaf ATP of illuminated leaves was not affected in ndufs8.1 ndufs8.2 (Fig. 3B), indicating either the activation of alternative mechanisms of ATP production as substrate-level phosphorylation at the level of mitochondrial enzymes, as proposed by Kühn et al (2015), or reduced rates of cellular processes resulting in a lower ATP consumption.…”

“…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.…”

“…In the N. sylvestris mutants, limited carbon supply resulting from higher photorespiration is likely to contribute to the slowgrowth phenotype (Priault et al, 2006b). Although similar metabolic alterations were observed in N. sylvestris (Dutilleul et al, 2005;Szal et al, 2008;Djebbar et al, 2012) and Arabidopsis CI mutants (Meyer et al, 2009;Keren et al, 2012) as increased levels of amino acids, ATP, and NAD(H), noteworthy differences were reported recently between Arabidopsis mutants (Kühn et al, 2015). Moreover, an increase in total reactive oxygen species (ROS) content was reported for many Arabidopsis CI mutants (Meyer et al, 2009;Keren et al, 2012;Soto et al, 2015) but not in the CMSII mutant (Dutilleul et al, 2003b).…”

“…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). Also, the growth defect of the Arabidopsis ca2 cal2 mutant was rescued under nonphotorespiratory conditions (Soto et al, 2015).…”

NAD Acts as an Integral Regulator of Multiple Defense Layers

“…Taken together, our results exemplify an important role of NAD in mitochondrial metabolism and stress. This is in line with studies on NAD-enriched mitochondrial mutants that were more tolerant to stress, including pathogens (Dutilleul et al, 2003(Dutilleul et al, , 2005Djebbar et al, 2012).…”