PMID- 38183796
OWN - NLM
STAT- MEDLINE
DCOM- 20240122
LR  - 20240201
IS  - 2213-2317 (Electronic)
IS  - 2213-2317 (Linking)
VI  - 69
DP  - 2024 Feb
TI  - Chloroplasts lacking class I glutaredoxins are functional but show a delayed 
      recovery of protein cysteinyl redox state after oxidative challenge.
PG  - 103015
LID - S2213-2317(23)00416-0 [pii]
LID - 10.1016/j.redox.2023.103015 [doi]
LID - 103015
AB  - Redox status of protein cysteinyl residues is mediated via glutathione 
      (GSH)/glutaredoxin (GRX) and thioredoxin (TRX)-dependent redox cascades. An 
      oxidative challenge can induce post-translational protein modifications on 
      thiols, such as protein S-glutathionylation. Class I GRX are small 
      thiol-disulfide oxidoreductases that reversibly catalyse S-glutathionylation and 
      protein disulfide formation. TRX and GSH/GRX redox systems can provide partial 
      backup for each other in several subcellular compartments, but not in the plastid 
      stroma where TRX/light-dependent redox regulation of primary metabolism takes 
      place. While the stromal TRX system has been studied at detail, the role of class 
      I GRX on plastid redox processes is still unknown. We generate knockout lines of 
      GRXC5 as the only chloroplast class I GRX of the moss Physcomitrium patens. While 
      we find that PpGRXC5 has high activities in GSH-dependent oxidoreductase assays 
      using hydroxyethyl disulfide or redox-sensitive GFP2 as substrates in vitro, 
      Deltagrxc5 plants show no detectable growth defect or stress sensitivity, in contrast 
      to mutants with a less negative stromal E(GSH) (Deltagr1). Using stroma-targeted 
      roGFP2, we show increased protein Cys steady state oxidation and decreased 
      reduction rates after oxidative challenge in Deltagrxc5 plants in vivo, indicating 
      kinetic uncoupling of the protein Cys redox state from E(GSH). Compared to 
      wildtype, protein Cys disulfide formation rates and S-glutathionylation levels 
      after H(2)O(2) treatment remained unchanged. Lack of class I GRX function in the 
      stroma did not result in impaired carbon fixation. Our observations suggest 
      specific roles for GRXC5 in the efficient transfer of electrons from GSH to 
      target protein Cys as well as negligible cross-talk with metabolic regulation via 
      the TRX system. We propose a model for stromal class I GRX function in efficient 
      catalysis of protein dithiol/disulfide equilibria upon redox steady state 
      alterations affecting stromal E(GSH) and highlight the importance of identifying 
      in vivo target proteins of GRXC5.
CI  - Copyright (c) 2024 The Authors. Published by Elsevier B.V. All rights reserved.
FAU - Bohle, Finja
AU  - Bohle F
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany; Chemical Signalling, Institute of Crop Science and 
      Resource Conservation (INRES), University of Bonn, D-53113, Bonn, Germany.
FAU - Rossi, Jacopo
AU  - Rossi J
AD  - Department of Pharmacy and Biotechnology, University of Bologna, I-40126, 
      Bologna, Italy.
FAU - Tamanna, Sadia S
AU  - Tamanna SS
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Jansohn, Hannah
AU  - Jansohn H
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Schlosser, Marlene
AU  - Schlosser M
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Reinhardt, Frank
AU  - Reinhardt F
AD  - Plant Physiology, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Brox, Alexa
AU  - Brox A
AD  - Crop Functional Genomics, Institute of Crop Science and Resource Conservation 
      (INRES), University of Bonn, D-53113, Bonn, Germany.
FAU - Bethmann, Stephanie
AU  - Bethmann S
AD  - Plant Biochemistry, Heinrich-Heine-University Dusseldorf, D-40225, Dusseldorf, 
      Germany.
FAU - Kopriva, Stanislav
AU  - Kopriva S
AD  - Institute for Plant Sciences, Cluster of Excellence on Plant Sciences (CEPLAS), 
      University of Cologne, Cologne, 50674, Germany.
FAU - Trentmann, Oliver
AU  - Trentmann O
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Jahns, Peter
AU  - Jahns P
AD  - Plant Biochemistry, Heinrich-Heine-University Dusseldorf, D-40225, Dusseldorf, 
      Germany.
FAU - Deponte, Marcel
AU  - Deponte M
AD  - Biochemistry, Department of Chemistry, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany.
FAU - Schwarzlander, Markus
AU  - Schwarzlander M
AD  - Institute of Plant Biology and Biotechnology, University of Munster, D-48143, 
      Munster, Germany.
FAU - Trost, Paolo
AU  - Trost P
AD  - Department of Pharmacy and Biotechnology, University of Bologna, I-40126, 
      Bologna, Italy.
FAU - Zaffagnini, Mirko
AU  - Zaffagnini M
AD  - Department of Pharmacy and Biotechnology, University of Bologna, I-40126, 
      Bologna, Italy.
FAU - Meyer, Andreas J
AU  - Meyer AJ
AD  - Chemical Signalling, Institute of Crop Science and Resource Conservation (INRES), 
      University of Bonn, D-53113, Bonn, Germany.
FAU - Muller-Schussele, Stefanie J
AU  - Muller-Schussele SJ
AD  - Molecular Botany, Department of Biology, RPTU Kaiserslautern-Landau, D-67633, 
      Kaiserslautern, Germany. Electronic address: mueschue@rptu.de.
LA  - eng
PT  - Journal Article
DEP - 20231228
PL  - Netherlands
TA  - Redox Biol
JT  - Redox biology
JID - 101605639
RN  - BBX060AN9V (Hydrogen Peroxide)
RN  - 0 (Glutaredoxins)
RN  - GAN16C9B8O (Glutathione)
RN  - 0 (Disulfides)
SB  - IM
MH  - *Hydrogen Peroxide/metabolism
MH  - *Glutaredoxins/genetics/metabolism
MH  - Oxidation-Reduction
MH  - Glutathione/metabolism
MH  - Oxidative Stress
MH  - Chloroplasts/metabolism
MH  - Disulfides/chemistry
PMC - PMC10808970
OTO - NOTNLM
OT  - E(GSH)
OT  - GRXC5
OT  - Genetically encoded biosensor
OT  - Glutaredoxin
OT  - Glutathione
OT  - Photosynthesis
OT  - Plastid
OT  - Redox-sensitive GFP
OT  - S-glutathionylation
COIS- Declaration of competing interest The authors declare that they have no known 
      competing financial interests or personal relationships that could have appeared 
      to influence the work reported in this paper.
EDAT- 2024/01/07 06:44
MHDA- 2024/01/22 06:43
PMCR- 2023/12/28
CRDT- 2024/01/06 18:05
PHST- 2023/11/12 00:00 [received]
PHST- 2023/12/08 00:00 [revised]
PHST- 2023/12/25 00:00 [accepted]
PHST- 2024/01/22 06:43 [medline]
PHST- 2024/01/07 06:44 [pubmed]
PHST- 2024/01/06 18:05 [entrez]
PHST- 2023/12/28 00:00 [pmc-release]
AID - S2213-2317(23)00416-0 [pii]
AID - 103015 [pii]
AID - 10.1016/j.redox.2023.103015 [doi]
PST - ppublish
SO  - Redox Biol. 2024 Feb;69:103015. doi: 10.1016/j.redox.2023.103015. Epub 2023 Dec 
      28.