ACHT4-driven oxidation of APS1 attenuates starch synthesis under low light intensity in Arabidopsis plants

Abstract

The regulatory mechanisms that use signals of low levels of reactive oxygen species (ROS) could be obscured by ROS produced under stress and thus are better investigated under homeostatic conditions. Previous studies showed that the chloroplastic atypical thioredoxin ACHT1 is oxidized by 2-Cys peroxiredoxin (2-Cys Prx) in Arabidopsis plants illuminated with growth light and in turn transmits a disulfide-based signal via yet unknown target proteins in a feedback regulation of photosynthesis. Here, we studied the role of a second chloroplastic paralog, ACHT4, in plants subjected to low light conditions. Likewise, ACHT4 reacted in planta with 2-Cys Prx, indicating that it is oxidized by a similar disulfide exchange reaction. ACHT4 further reacted uniquely with the small subunit (APS1) of ADP-glucose pyrophosphorylase (AGPase), the first committed enzyme of the starch synthesis pathway, suggesting that it transfers the disulfides it receives from 2-Cys Prx to APS1 and turns off AGPase. In accordance, ACHT4 participated in an oxidative signal that quenched AGPase activity during the diurnal transition from day to night, and also in an attenuating oxidative signal of AGPase in a dynamic response to small fluctuations in light intensity during the day. Increasing the level of expressed ACHT4 or of ACHT4 ΔC , a C terminus-deleted form that does not react with APS1, correspondingly decreased or increased the level of reduced APS1 and decreased or increased transitory starch content. These findings imply that oxidative control mechanisms act in concert with reductive signals to fine tune starch synthesis during daily homeostatic conditions. oxidative signal | homeostasis | light intensity regulation | starch synthesis | chloroplast

Diurnal fluctuations in chloroplast GSH redox state regulate susceptibility to oxidative stress and cell fate in a bloom‐forming diatom

“…A similar phenomenon was recently reported in Arabidopsis where re‐oxidation of the chloroplast atypical thioredoxin (ACHT4) by peroxiredoxin occurred shortly following illumination, playing a role in regulation of starch biosynthesis (Eliyahu et al. ). It is possible that the observed oxidative burst is a result of oxygen reduction by the Mehler reaction (also known as the water–water reaction) which is important for light dissipation when the Calvin cycle is not fully functional and needs light‐dependent activation (Makino et al.…”

“…), similar to light‐induced peroxiredoxin oxidation in plants (Eliyahu et al. ), indicating a critical role of oxidative signaling in addition to the reductive signaling.…”

“…Diatoms can also regulate ATP/ NADPH ratio through rerouting of reducing power from the chloroplast to the mitochondria and import of mitochondrial ATP to the plastid under fluctuating light regimes, exemplifying the unique plasticity of diatom's rapid acclimation (Bailleul et al 2015). We suggest that this oxidative burst serves as a daily oxidative signal which affects the regulation of redox-sensitive protein networks (Rosenwasser et al 2014), similar to light-induced peroxiredoxin oxidation in plants (Eliyahu et al 2015), indicating a critical role of oxidative signaling in addition to the reductive signaling.…”

Photosynthate partitioning to starch in Arabidopsis thaliana is insensitive to light intensity but sensitive to photoperiod due to a restriction on growth in the light in short photoperiods

“…Activation is mediated by thioredoxin f1 (TRXf1) in response to light (Thormählen et al 2013) and the dual function NADPH-thioredoxin reductase C (NTRC) in response to sugar (Michalska et al 2009;Thormählen et al 2013). Starch accumulation is only marginally affected in the ntrc mutant (Li et al 2012) but is decreased in a trxf1 mutant (Thormählen et al 2013) and more severely in a trxf ntrc double mutant (Thormählen et al 2015), and ACHT4-driven oxidation of the small subunit of AGPase (APS1) attenuated starch synthesis under very low light intensity (Eliyahu et al 2015). However, these effects on starch accumulation may be in part indirect.…”

Multi‐level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance

“…In the light, electron flow from photosystem I (PSI) leads to reduction of ferredoxin (Fd), which can reduce Trx via FTR and in turn reduce the disulfides on target enzymes. In the dark, free thiols are re‐oxidized, possibly through the action of specific enzymes such as the chloroplastic atypical thioredoxin (ACHT4), reversing the regulatory processes (Eliyahu et al ., ).…”