Mitochondrial Dihydrolipoyl Dehydrogenase Activity Shapes Photosynthesis and Photorespiration of Arabidopsis thaliana

Abstract

Mitochondrial dihydrolipoyl dehydrogenase (mtLPD; L-protein) is an integral component of several multienzyme systems involved in the tricarboxylic acid (TCA) cycle, photorespiration, and the degradation of branched-chain a-ketoacids. The majority of the mtLPD present in photosynthesizing tissue is used for glycine decarboxylase (GDC), necessary for the high-flux photorespiratory glycine-into-serine conversion. We previously suggested that GDC activity could be a signal in a regulatory network that adjusts carbon flux through the Calvin-Benson cycle in response to photorespiration. Here, we show that elevated GDC L-protein activity significantly alters several diagnostic parameters of cellular metabolism and leaf gas exchange in Arabidopsis thaliana. Overexpressor lines displayed markedly decreased steady state contents of TCA cycle and photorespiratory intermediates as well as elevated NAD(P) + -to-NAD(P)H ratios. Additionally, increased rates of CO 2 assimilation, photorespiration, and plant growth were observed. Intriguingly, however, day respiration rates remained unaffected. By contrast, respiration was enhanced in the first half of the dark phase but depressed in the second. We also observed enhanced sucrose biosynthesis in the light in combination with a lower diel magnitude of starch accumulation and breakdown. These data thus substantiate our prior hypothesis that facilitating flux through the photorespiratory pathway stimulates photosynthetic CO 2 assimilation in the Calvin-Benson cycle. They furthermore suggest that this regulation is, at least in part, dependent on increased light-capture/use efficiency.

On the role of the tricarboxylic acid cycle in plant productivity

“…As one of the most abundant mitochondrial proteins, this enzyme has for many decades been the subject of detailed study (Douce et al ). Arabidopsis knockouts of the L‐protein, a mitochondrial dihydrolipoyl dehydrogenase that mainly participates in the glycine decarboxylase complex, revealed that they were characterized by reduced levels of TCA cycle and photorespiratory intermediates, yet they had enhanced rates of photosynthesis and growth (Timm et al ). Collectively, these examples underscore the importance of mitochondrial reactions in proper chloroplast, and hence cellular function, and highlight that the manipulation of certain steps of the pathway can result in enhanced aerial growth, and indeed, crop yield.…”

Proteome Analysis Reveals Extensive Light Stress-Response Reprogramming in the Seagrass Zostera muelleri (Alismatales, Zosteraceae) Metabolism

“…Furthermore, plants under SSL conditions exhibited the up-regulation of glutamate-ammonia ligase (also recognized as glutamine synthetase, GS), an enzyme that assimilates the ammonia generated in the GCC via the GS/GOGAT cycle by consuming reducing equivalents from ferrodoxin and/or NADPH/ATP. In turn, up-regulation of mtLPD, HPR, and GCC activity suggest that the plants under SSL conditions were regulating the photorespiratory carbon cycle, effectively shaping photosynthesis (Timm et al, 2015). This allows for increased performance of the C3 cycle and enhance the generation of ribulose-1,5-bisphosphate (RuBP), also facilitating the consumption of photorespiratory metabolites and, in turn, photosynthetic carbon assimilation (Voss et al, 2013).…”

The Sclerophyllous Eucalyptus camaldulensis and Herbaceous Nicotiana tabacum Have Different Mechanisms to Maintain High Rates of Photosynthesis

“…A reduction in C c also accelerates the production of photorespiratory intermediates, e.g., glycine and glycerate, which inhibit the Calvin-Benson cycle (Chastain and Ogren, 1989; Eisenhut et al, 2007; Timm et al, 2012, 2015). In Arabidopsis thaliana plants with elevated glycine decarboxylase activity, the rapid acceleration of the photorespiratory pathway lowers the accumulation of photorespiratory metabolites including those which impair Rubisco activation and possibly the activity of other enzymes of the Calvin-Benson cycle, increasing the performance of the Calvin-Benson cycle (Timm et al, 2012, 2015).…”

“…In Arabidopsis thaliana plants with elevated glycine decarboxylase activity, the rapid acceleration of the photorespiratory pathway lowers the accumulation of photorespiratory metabolites including those which impair Rubisco activation and possibly the activity of other enzymes of the Calvin-Benson cycle, increasing the performance of the Calvin-Benson cycle (Timm et al, 2012, 2015). Furthermore, N. tabacum plants grown under high light and high nitrogen concentration up-regulate photorespiratory pathway to maintain high rates of photosynthesis (Huang et al, 2014, 2016).…”

“…Enhancement of the photorespiratory pathway leads to a considerably improved net photosynthetic rate in Arabidopsis thaliana (Timm et al, 2012, 2015). Therefore, we might also speculate that E. camaldulensis enhances the capacity of that pathway to favor the Calvin-Benson cycle.…”