TY - JOUR
T1 - Systematic monitoring of 2-Cys peroxiredoxin-derived redox signals unveiled its role in attenuating carbon assimilation rate
AU - Lampl, Nardy
AU - Lev, Raz
AU - Nissan, Idan
AU - Gilad, Gal
AU - Hipsch, Matanel
AU - Rosenwasser, Shilo
N1 - Publisher Copyright:
Copyright © 2022 the Author(s).
PY - 2022/6/7
Y1 - 2022/6/7
N2 - 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.
AB - 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.
KW - biosensor
KW - chloroplast
KW - oxidative signal
KW - peroxiredoxin
KW - photosynthesis
UR - http://www.scopus.com/inward/record.url?scp=85131271018&partnerID=8YFLogxK
U2 - 10.1073/pnas.2119719119
DO - 10.1073/pnas.2119719119
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C2 - 35648819
AN - SCOPUS:85131271018
SN - 0027-8424
VL - 119
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 23
M1 - e2119719119
ER -