A Chloroplast Light-Regulated Oxidative Sensor for Moderate Light Intensity in Arabidopsis

Abstract

The transition from dark to light involves marked changes in the redox reactions of photosynthetic electron transport and in chloroplast stromal enzyme activity even under mild light and growth conditions. Thus, it is not surprising that redox regulation is used to dynamically adjust and coordinate the stromal and thylakoid compartments. While oxidation of regulatory proteins is necessary for the regulation, the identity and the mechanism of action of the oxidizing pathway are still unresolved. Here, we studied the oxidation of a thylakoid-associated atypical thioredoxin-type protein, ACHT1, in the Arabidopsis thaliana chloroplast. We found that after a brief period of net reduction in plants illuminated with moderate light intensity, a significant oxidation reaction of ACHT1 arises and counterbalances its reduction. Interestingly, ACHT1 oxidation is driven by 2-Cys peroxiredoxin (Prx), which in turn eliminates peroxides. The ACHT1 and 2-Cys Prx reaction characteristics in plants further indicated that ACHT1 oxidation is linked with changes in the photosynthetic production of peroxides. Our findings that plants with altered redox poise of the ACHT1 and 2-Cys Prx pathway show higher nonphotochemical quenching and lower photosynthetic electron transport infer a feedback regulatory role for this pathway.

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

“…6, its intermolecular disulfide reaction intermediates. Protein blot analysis of denatured, but not reduced, plant extracts identified three intermolecular disulfide-linked ACHT4-containing protein complexes, verified by their susceptibility to chemical reduction by DTT (Fig.…”

“…chloroplast-localized Trxs that have an atypical redox-active site, and a less reducing redox midpoint potential than that of canonical chloroplast Trxs, and that were shown to be good catalysts of 2-Cys Prx reduction, but not of malate dehydrogenase, in vitro (19). Study of the thylakoids-associated ACHT1 revealed that it transmits a disulfide-based oxidative signal in feedback regulation of photosynthesis under homeostasis growth conditions (6). ACHT1 oxidation is driven by 2-Cys Prx, a peroxidase with a low K m for hydrogen peroxide (20)(21)(22) that is conceivably required for the low level of ROS that are typical in signaling events.…”

“…ACHT1 undergoes rapid redox state changes during the transition of plants from dark to light and afterward, such that, after a short period of net reduction, the ACHT1 pool is maintained in a partially oxidized state in the light. Thus, a mechanism through which ACHT1, together with 2-Cys Prx, transmits an oxidative signal in response to illumination of plants with normal light intensity was proposed (6).…”

“…Similarly, rapid changes in light intensity throughout the day serve as environmental cues fine tuning such processes. Perhaps because of the short response time required to keep photosynthesis-derived reactive oxygen species (ROS) from becoming harmful, plants use redox signals as a direct and dynamic means of regulating multiple posttranscriptional events and alleviating damage (1)(2)(3)(4)(5)(6)(7).…”

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

“…These molecules comprise the reductive pool of the cell and react directly with oxidizing agents or through enzymatic reactions mediated by the different antioxidant enzymes listed above (Mittler, 2002). Controlled by the cellular antioxidant system, ROS is a key signaling factor that mediates acclimation responses to environmental stress conditions (Foyer and Noctor, 2003;Mittler et al, 2004;D'Autréaux and Toledano, 2007;Dangoor et al, 2012). Recent reports proposed an important role for ROS metabolism in algal response to environmental stress, such as iron limitation, allelopathy, UV stress, photo-acclimation and oxidative stress (Rijstenbil, 2002;Sukenik et al, 2002;Vardi et al, 2002Vardi et al, , 2007Janknegt et al, 2008;Li et al, 2009;Murik and Kaplan, 2009;Fischer et al, 2012;Thamatrakoln et al, 2012;Graff van Creveld et al, 2014;Murik et al, 2014).…”