Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement

Abstract

The MSC16 cucumber (Cucumis sativus L.) mutant with lower activity of mitochondrial Complex I was used to study the influence of mitochondrial metabolism on whole cell energy and redox state. Mutant plants had lower content of adenylates and NADP(H) whereas the NAD(H) pool was similar as in wild type. Subcellular compartmentation of adenylates and pyridine nucleotides were studied using the method of rapid fractionation of protoplasts. The data obtained demonstrate that dysfunction of mitochondrial respiratory chain decreased the chloroplastic ATP pool. No differences in NAD(H) pools in subcellular fractions of mutated plants were observed; however, the cytosolic fraction was highly reduced whereas the mitochondrial fraction was more oxidized in MSC16, as compared to WTc. The NADP(H) pool in MSC16 protoplasts was greatly decreased and the chloroplastic NADP(H) pool was more reduced, whereas the extrachloroplastic pool was much more oxidized, than in WTc protoplast. Changes in nucleotides distribution in cucumber MSC16 mutant were compared to changes found in tobacco (Nicotiana sylvestris) CMS II mitochondrial mutant. In contrast to MSC16 cucumber, the content of adenylates in tobacco mutant was much higher than in tobacco wild type. The differences were more pronounced in leaf tissue collected after darkness than in the middle of the photoperiod. Results obtained after tobacco protoplast fractionating showed that the increase in CMS II adenylate content was mainly due to a higher level in extrachloroplast fraction. Both mutations have a negative effect on plant growth through perturbation of chloroplast/mitochondrial interactions.

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 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).…”

Intracellular Redox Compartmentation and ROS-Related Communication in Regulation and Signaling

“…Based on information obtained using these approaches, Table I presents values for ascorbate, glutathione, and pyridine nucleotide concentrations and reduction states (Heineke et al, 1991;Igamberdiev and Gardeström, 2003;Szal et al, 2008;Zechmann et al, 2008Zechmann et al, , 2011Queval et al, 2011;Smirnoff, 2011). Notable features are as follows: (1) ascorbate is highly reduced in all compartments apart from the vacuole and apoplast, where DHA can accumulate either because of ascorbate oxidase or because of the lack of regeneration systems; (2) like ascorbate, glutathione in extracts is highly reduced in the absence of stress; indeed, in situ analysis suggests that the reduction state is very high in many compartments (Meyer et al, 2007), with most of the GSSG present in the vacuole or apoplast; and (3) pyridine nucleotide pools are poised at more reduced states in the mitochondria than in the cytosol and chloroplast, which contain more oxidized pools.…”

“…d Nonaqueous or rapid fractionation (Heineke et al, 1991;Igamberdiev and Gardeströ m, 2003;Szal et al, 2008).…”

The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis

“…Low concentrations of malate and fumarate lead to accelerated dark-induced senescence in a malic enzyme-overexpressing Arabidopsis line, while sugar levels are high (Fahnenstich et al, 2007). Down-regulation of different respiratory chain complexes restricts growth despite unchanged or even increased steady-state ATP levels (Szal et al, 2008;Robison et al, 2009;Geisler et al, 2012). The high AMP-ATP ratio in ethe1-1 plants could induce a broad transcriptional response to stress and energy deprivation mediated by AMP-activated protein kinases such as KIN10 (AT3G01090), which is coexpressed with ETHE1 (Baena- González et al, 2007).…”