Systematic monitoring of 2-Cys peroxiredoxin-derived redox signals unveiled its role in attenuating carbon assimilation rate

Nardy Lampl, Raz Lev, Idan Nissan, Gal Gilad, Matanel Hipsch, Shilo Rosenwasser*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Transmission of reductive and oxidative cues from the photosynthetic electron transport chain to redox regulatory protein networks plays a crucial role in coordinating photosynthetic activities. The tight balance between these two signals dictates the cellular response to changing light conditions. While the role of reductive signals in activating chloroplast metabolism is well established, the role of their counterbalanced oxidative signals is still unclear, mainly due to monitoring difficulties. Here, we introduced chlroGFP2-PrxΔCR, a 2-Cys peroxiredoxin-based biosensor, into Arabidopsis thaliana chloroplasts to monitor the dynamic changes in photosynthetically derived oxidative signaling. We showed that chl-roGFP2-PrxΔCR oxidation states reflected oxidation patterns similar to those of endogenous 2-Cys peroxiredoxin under varying light conditions. By employing a set of genetically encoded biosensors, we showed the induction of 2-Cys peroxiredoxin-dependent oxidative signals, throughout the day, under varying light intensities and their inverse relationship with NADPH levels, unraveling the combined activity of reducing and oxidizing signals. Furthermore, we demonstrated the induction of 2-Cys peroxiredoxin-derived oxidative signals during a dark–to–low-light transition and uncovered a faster increase in carbon assimilation rates during the photosynthesis induction phase in plants deficient in 2-Cys peroxiredoxins compared with wild type, suggesting the involvement of oxidative signals in attenuating photosynthesis. The presented data highlight the role of oxidative signals under nonstress conditions and suggest that oxidative signals measured by peroxiredoxin-based biosensors reflect the limitation to photosynthesis imposed by the redox regulatory system.

Original languageEnglish
Article numbere2119719119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number23
DOIs
StatePublished - 7 Jun 2022

Bibliographical note

Publisher Copyright:
Copyright © 2022 the Author(s).

Keywords

  • biosensor
  • chloroplast
  • oxidative signal
  • peroxiredoxin
  • photosynthesis

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