Redox regulation of the Calvin–Benson cycle: something old, something new

Abstract

Reversible redox post-translational modifications such as oxido-reduction of disulfide bonds, S-nitrosylation, and S-glutathionylation, play a prominent role in the regulation of cell metabolism and signaling in all organisms. These modifications are mainly controlled by members of the thioredoxin and glutaredoxin families. Early studies in photosynthetic organisms have identified the Calvin–Benson cycle, the photosynthetic pathway responsible for carbon assimilation, as a redox regulated process. Indeed, 4 out of 11 enzymes of the cycle were shown to have a low activity in the dark and to be activated in the light through thioredoxin-dependent reduction of regulatory disulfide bonds. The underlying molecular mechanisms were extensively studied at the biochemical and structural level. Unexpectedly, recent biochemical and proteomic studies have suggested that all enzymes of the cycle and several associated regulatory proteins may undergo redox regulation through multiple redox post-translational modifications including glutathionylation and nitrosylation. The aim of this review is to detail the well-established mechanisms of redox regulation of Calvin–Benson cycle enzymes as well as the most recent reports indicating that this pathway is tightly controlled by multiple interconnected redox post-translational modifications. This redox control is likely allowing fine tuning of the Calvin–Benson cycle required for adaptation to varying environmental conditions, especially during responses to biotic and abiotic stresses.

Defects in a New Class of Sulfate/Anion Transporter Link Sulfur Acclimation Responses to Intracellular Glutathione Levels and Cell Cycle Control

“…It is well known that light reactions of photosynthesis generate abundant reactive oxygen species (Balsera et al, 2014;Schmitt et al, 2014) and may activate the transcription of SMT15 in order to maintain glutathione homeostasis and thereby mitigate cellular damage and stress caused by reactive oxygen species. Equally possible is that glutathione levels are directly coupled to the glutathionylation/deglutathionylation of proteins required for photosynthetic activities as cells grow (Zaffagnini et al, 2012;Michelet et al, 2013).…”

Thioredoxin and NADPH-Dependent Thioredoxin Reductase C Regulation of Tetrapyrrole Biosynthesis

“…In higher plants, the plastid-localized TRX family can be classified into five subgroups, including two f-type (TRX f1 and f2), four m-type (TRX m1-m4), one x-type (TRX x), two y-type (TRX y1 and y2), and one z-type (TRX z) TRX isoforms (Michalska et al, 2009;Michelet et al, 2013;Serrato et al, 2013;Balsera et al, 2014). Numerous in vitro and in vivo studies have shown that TRX f and TRX m are required for multiple metabolic processes in chloroplasts, including the Calvin-Benson cycle (Collin et al, 2003;Michelet et al, 2013;Okegawa and Motohashi, 2015;Yoshida et al, 2015), ATP synthesis (Schwarz et al, 1997) and NADPH export (Wolosiuk et al, 1979;Lara et al, 1980), starch metabolism (Fu et al, 1998;Mikkelsen et al, 2005;Seung et al, 2013;Thormählen et al, 2013), fatty acid synthesis (Sasaki et al, 1997), amino acid synthesis (Balmer et al, 2003), and chlorophyll (Chl) synthesis (Ikegami et al, 2007;Luo et al, 2012).…”

Photosynthesis of microalgae in outdoor mass cultures and modelling its effects on biomass productivity for fuels, feeds and chemicals

“…Deactivation of CBB cycle enzymes is thought to prevent photorespiration of carbon in the absence of NADPH, which would waste ATP in the process. In fact, recent biochemical and proteomic studies have indicated that all 11 enzymes as well as several associated regulatory proteins of the CBB cycle may be redox regulated (Michelet et al, 2013).…”

“…In addition to energy dissipation, zeaxanthin plays a major role in ROS scavenging and detoxification (Dall'Osto et al, 2010). Additional ROS detoxification is mediated by glutathione peroxidases, peroxiredoxins and methionine sulfoxide reductases which are regenerated by thioredoxins (Michelet et al, 2013). …”

“…Key enzymes regulated by thioredoxins include four directly involved in the CBB cycle (phosphoribulokinase, glyceraldehyde-3-phosphate dehydrogenase, fructose-1,6-bisphosphatase, and sedoheptulose-1,7-bisphosphatase); ATP synthase; Acetyl-CoAcarboxylase, involved in initial steps of fatty acid synthesis, and three enzymes involved in starch metabolic pathways (ADPglucosepyrophosphorylase, glucan:water dikinase and beta-amylase BAM1 (Michelet et al, 2013). Moreover, a proteomics study revealed a total of 55 possible protein targets of thioredoxins in C.…”