A Deficiency in the Flavoprotein of Arabidopsis Mitochondrial Complex II Results in Elevated Photosynthesis and Better Growth in Nitrogen-Limiting Conditions    

Abstract

Mitochondrial complex II (succinate dehydrogenase [SDH]) plays roles both in the tricarboxylic acid cycle and the respiratory electron transport chain. In Arabidopsis (Arabidopsis thaliana), its flavoprotein subunit is encoded by two nuclear genes, SDH1-1 and SDH1-2. Here, we characterize heterozygous SDH1-1/sdh1-1 mutant plants displaying a 30% reduction in SDH activity as well as partially silenced plants obtained by RNA interference. We found that these plants displayed significantly higher CO 2 assimilation rates and enhanced growth than wild-type plants. There was a strong correlation between CO 2 assimilation and stomatal conductance, and both mutant and silenced plants displayed increased stomatal aperture and density. By contrast, no significant differences were found for dark respiration, chloroplastic electron transport rate, CO 2 uptake at saturating concentrations of CO 2 , or biochemical parameters such as the maximum rates of carboxylation by Rubisco and of photosynthetic electron transport. Thus, photosynthesis is enhanced in SDH-deficient plants by a mechanism involving a specific effect on stomatal function that results in improved CO 2 uptake. Metabolic and transcript profiling revealed that mild deficiency in SDH results in limited effects on metabolism and gene expression, and data suggest that decreases observed in the levels of some amino acids were due to a higher flux to proteins and other nitrogen-containing compounds to support increased growth. Strikingly, SDH1-1/ sdh1-1 seedlings grew considerably better in nitrogen-limiting conditions. Thus, a subtle metabolic alteration may lead to changes in important functions such as stomatal function and nitrogen assimilation.

Responses to Light Intensity in a Genome-Scale Model of Rice Metabolism

“…This ability of the TCA cycle reactions in plants to reconfigure to fulfill different needs has also been pointed out by other authors , and some of the flux patterns shown in that paper can be seen in Figure 4. Also, the phenotypes of transgenic plants with reduced activities of succinate dehydrogenase and fumarase are different; tomato plants with fumarase reduced sufficiently to inhibit mitochondrial respiration have a reduced rate of photosynthesis and growth (Nunes-Nesi et al, 2007), while the opposite is the case for tomato and Arabidopsis with reduced succinate dehydrogenase Fuentes et al, 2011). In both cases, the primary mechanism of the effect is reported to be through effects on stomatal conductance, possibly caused by metabolite signaling to the guard cells, rather than an effect on photosynthetic capacity.…”

SDH6 and SDH7 Contribute to Anchoring Succinate Dehydrogenase to the Inner Mitochondrial Membrane in Arabidopsis thaliana

“…Knock out of genes encoding SDH1 or SDH2 caused a failure of gametophyte development (León et al, 2007;Huang and Millar, 2013). Down-regulation of SDH genes led to increased succinate levels as well as altered concentrations of organic acids and amino acids Fuentes et al, 2011). It was shown recently that complex II is a site of reactive oxygen species production in plants (Gleason et al, 2011;Jardim-Messeder et al, 2015).…”

Decreasing the Mitochondrial Synthesis of Malate in Potato Tubers Does Not Affect Plastidial Starch Synthesis, Suggesting That the Physiological Regulation of ADPglucose Pyrophosphorylase Is Context Dependent

“…They were additionally characterized by clearly decreased starch contents in the case of the fumarase antisense lines (Nunes-Nesi et al, 2007) and increased contents in the malate dehydrogenase and succinate dehydrogenase antisense lines. Although a similar pattern was not seen in the succinate dehydrogenase knockout mutant of Arabidopsis (Arabidopsis thaliana; Fuentes et al, 2011), it is important to note that the level of malate was not altered in this mutant. Unfortunately, the effect of knocking out both mitochondrial isoforms of malate dehydrogenase in Arabidopsis on starch levels was not documented (Tomaz et al, 2010); however, knocking out the cytosolic fumarase of Arabidopsis resulted in a high-starch leaf phenotype .…”