Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition

Abstract

The possible role of L-ascorbate (AsA) as a biochemical signal during the interactions between photosynthesis and respiration was examined in leaf discs of Arabidopsis thaliana. AsA content was either decreased as in AsA-deficient vtc1 mutants or increased by treatment with L-galactono-1, 4-lactone (L-GalL, a precursor of AsA; EC 1.3.2.3). In mutants, photosynthesis was extremely sensitive to both antimycin A (inhibitor of the cytochrome c oxidase pathway [COX pathway]) and salicylhydroxamic acid (SHAM, inhibitor of the alternative pathway [AOX pathway]), particularly at high light conditions. Mitochondrial inhibitors lowered the ratio of reduced AsA to total AsA, at high light, indicating oxidative stress in leaf discs. Elevation of AsA by L-GalL decreased the sensitivity of photosynthesis at high light to antimycin A or SHAM, sustained photosynthesis at supraoptimal light and relieved the extent of photoinhibition. High ratios of reduced AsA to total AsA in L-GalL-treated leaf discs suggests that L-GalL lowers oxidative stress. The protection by L-GalL of photosynthesis against the mitochondrial inhibitors and photoinhibition was quite pronounced in vtc1 mutants. Our results suggest that the levels and redox state of AsA modify the pattern of modulation of photosynthesis by mitochondrial metabolism. The extent of the AOX pathway as a percentage of the total respiration in Arabidopsis mesophyll protoplasts was much higher in vtc1 than in wild type. We suggest that the role of AsA becomes pronounced at high light and/or when the AOX pathway is inhibited. While acknowledging the importance of the COX pathway, we hypothesize that AsA and the AOX pathway may complement each other to protect photosynthesis against photoinhibition.

The Inter-Relationship of Ascorbate Transport, Metabolism and Mitochondrial, Plastidic Respiration

“…However, the photoinhibition-even in the presence of antimycin A or SHAM-could be decreased significantly by the treatment with L-galactono-1,4-lactone. As was expected, the protective effect of L-galactono-1,4-lactone was maximal in vtc-1 mutants in the presence of SHAM (49).…”

“…Ascorbate can be an important element of the photosynthetic ETC, mETC, and TCA cycle regulatory network since (i) the level of ascorbate can influence the intensity of photosynthesis (35,38,49); (ii) the electron flux through the photosynthetic ETC influences the biosynthesis of ascorbate (55); (iii) ascorbate is synthesized tightly coupled to the mETC by providing electrons to complex IV (7) in case of the inhibition of TCA cycle (38) and (iv) the activity of AOX also influences the biosynthetic rate of ascorbate (8). Any changes in either of these elements of this network influence the others (Fig.…”

“…Furthermore, the restriction of mitochondrial electron transport decreased the ratio of the reduced form of both ascorbate and GSH (16). Accordingly, the application of these respiratory inhibitors in vtc-1 mutant Arabidopsis caused an extreme level of photoinhibition (83%) (49). However, the photoinhibition-even in the presence of antimycin A or SHAM-could be decreased significantly by the treatment with L-galactono-1,4-lactone.…”

Mitochondrial Energy and Redox Signaling in Plants

“…This suggests that ABI4 plays a role in low ascorbate signaling, most likely by modulating abscisic acid (ABA) levels (94). Respiration-dependent changes in mitochondrial ascorbate synthesis may modulate interorganellar communication between plastids and mitochondria (214) and could regulate RTG signaling as a common signal from both organelles. Further dissection of the signaling mechanisms upstream of ABI4 will need to elucidate the role of ascorbate in RTG crosstalk.…”

Ascorbate metabolism in vegetative and reproductive organs of "cherry" tomato

“…AsA redox reactions are often referred to in literature as ascorbate-glutathione circle, which plays an important role in plants in redox status regulation through the activity of four enzymes; ascorbate Peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR), encoded by multigene families (Mittler 2002). AsA is mostly associated to various biotic and abiotic stresses including pathogens, drought and oxidizing agents and also to the regulation of chloroplast-mitochondria interactions in photosynthetic cells (Conklin, Barth 2004;Fotopoulos et al 2008;Smirnoff 2011;Talla et al 2011). AsA also acts as a co-factor and protects sev-eral enzymes with active sites susceptible to oxidation (Prescott, John 1996).…”