Thioredoxin h2 contributes to the redox regulation of mitochondrial photorespiratory metabolism

Abstract

Thioredoxins (TRXs) are important proteins involved in redox regulation of metabolism. In plants, it has been shown that the mitochondrial metabolism is regulated by the mitochondrial TRX system. However, the functional significance of TRX h2, which is found at both cytosol and mitochondria, remains unclear. Arabidopsis plants lacking TRX h2 showed delayed seed germination and reduced respiration alongside impaired stomatal and mesophyll conductance, without impacting photosynthesis under ambient O2 conditions. However, an increase in the stoichiometry of photorespiratory CO2 release was found during O2‐dependent gas exchange measurements in trxh2 mutants. Metabolite profiling of trxh2 leaves revealed alterations in key metabolites of photorespiration and in several metabolites involved in respiration and amino acid metabolism. Decreased abundance of serine hydroxymethyltransferase and glycine decarboxylase (GDC) H and L subunits as well as reduced NADH/NAD+ ratios were also observed in trxh2 mutants. We further demonstrated that the redox status of GDC‐L is altered in trxh2 mutants in vivo and that recombinant TRX h2 can deactivate GDC‐L in vitro, indicating that this protein is redox regulated by the TRX system. Collectively, our results demonstrate that TRX h2 plays an important role in the redox regulation of mitochondrial photorespiratory metabolism.

Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism

“…Indirect evidence that photorespiration is not all wasteful, however, comes from photorespiratory mutant studies. As discussed above, λ values deviating from 0.5 have been previously observed experimentally (Hanson and Peterson, , ; Cousins et al , ; Timm et al , ; Cousins et al , ; Walker and Cousins, ; da Fonseca‐Pereira et al , ), which would be expected if carbon is exported from the photorespiratory pathway. These observations hint at an important role of the photorespiratory pathway in supplying the demand for metabolites for other processes and that it acts as an open pathway, rather than a closed cycle, when rates of oxygenation are not exceeding this demand.…”

“…In their early attempt to measure the stoichiometry of photorespiratory CO 2 release per oxygenation reaction in vivo they determined values ranging from 0.30 to 0.84, depending on environmental conditions such as temperature and light intensity. Since then, other studies have reported a departure of λ from 0.5 in mutants that had an impairment in the photorespiratory pathway, such as plants lacking peroxisomal malate dehydrogenase (PMDH; Cousins et al , ), HPR1 (Timm et al , ; Cousins et al , ), or thioredoxins THX h2 or THX o1 (da Fonseca‐Pereira et al , ; Reinholdt et al , ), and in wild‐type tobacco, wheat, soybean, and Arabidopsis (Walker and Cousins, ; Walker et al , ). A value of λ lower than 0.5 would be expected if carbon is diverted from the photorespiratory pathway as glycine (Busch et al , ).…”

Redox-Regulation of Photorespiration through Mitochondrial Thioredoxin o1

“…It is known that TRXh2 is also present in mitochondria (Daloso et al, 2015), and we currently cannot rule out some redundancy between these two proteins, thus weakening the phenotype of the single trxo1 mutant. Interestingly, da Fonseca-Pereira et al (2019) reported that loss of TRXh2 also impacts photorespiration and is also able to redox-regulate LPD. Given changes in the phosphorylated pyridine nucleotide contents during CO 2 transition are most dominant in the trxo1 and TxGT mutants shortly after transfer into normal air (Fig.…”

Thioredoxin Network in Plant Mitochondria: Cysteine S-Posttranslational Modifications and Stress Conditions

“…It was concluded that TRX o 1 contributes to adjust photorespiration in response to environmental fluctuations via the regulation of GDC and possibly other mitochondrial multienzyme systems in which LPD is involved ( Reinholdt et al, 2019a ). Not only TRX o 1, but also AtTRX h 2, contributes to the redox regulation of mitochondrial photorespiratory metabolism ( Da Fonseca-Pereira et al, 2019a ) ( Figure 2 ). AtTRX h 2 regulates the redox state of GDC-L protein, which is altered in trxh2 mutants in vivo .…”