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Peroxiredoxins and Redox Signaling in Plants - PubMed

  • ️Mon Jan 01 2018

Review

Peroxiredoxins and Redox Signaling in Plants

Michael Liebthal et al. Antioxid Redox Signal. 2018.

Abstract

Significance: Peroxiredoxins (Prxs) are thiol peroxidases with multiple functions in the antioxidant defense and redox signaling network of the cell. Our progressing understanding assigns both local and global significance to plant Prxs, which are grouped in four Prx types. In plants they are localized to the cytosol, mitochondrion, plastid, and nucleus. Antioxidant defense is fundamentally connected to redox signaling, cellular communication, and acclimation. The thiol-disulfide network is central part of the stress sensing and processing response and integrates information input with redox regulation. Recent Advances: Prxs function both as redox sensory system within the network and redox-dependent interactors. The processes directly or indirectly targeted by Prxs include gene expression, post-transcriptional reactions, including translation, post-translational regulation, and switching or tuning of metabolic pathways, and other cell activities. The most advanced knowledge is available for the chloroplast 2-CysPrx wherein recently a solid interactome has been defined. An in silico analysis of protein structure and coexpression reinforces new insights into the 2-CysPrx functionality.

Critical issues: Up to now, Prxs often have been investigated for local properties of enzyme activity. In vitro and ex vivo work with mutants will reveal the ability of Prxs to interfere with multiple cellular components, including crosstalk with Ca2+-linked signaling pathways, hormone signaling, and protein homeostasis.

Future directions: Complementation of the Prxs knockout lines with variants that mimic specific states, namely devoid of peroxidase activity, lacking the oligomerization ability, resembling the hyperoxidized decamer, or with truncated C-terminus, should allow dissecting the roles as thiol peroxidase, oxidant, interaction partner, and chaperone. Antioxid. Redox Signal. 28, 609-624.

Keywords: 2-cysteine peroxiredoxin; chloroplast; interactome; post-translational modifications; redox network; signaling; thiol peroxidase.

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Figures

<b>FIG. 1.</b>
FIG. 1.

Peroxide binding pocket with conserved amino acids. (A) Graphical presentation of the catalytic center of the mitochondrial PrxIIF of pea. The template was accessed from RCSB PDB with the model of 2PWJ (2007) at 2.8 Å resolution. The conserved amino acids CysP 87, Arg 165, Thr 84, and Pro 80 are depicted using PyMOL (29). The peroxyl moiety was placed in appropriate position in the catalytic reaction pocket to simulate peroxide binding. (B) Potential surface mesh is laid on the active site residues and the terminal oxygen of substrate.

<b>FIG. 2.</b>
FIG. 2.

Schematics of the peroxidase cycle and hyperoxidation cycle of Prxs. (I) Reduced Prx scavenges peroxides (H2O2) releasing water. The peroxidatic cysteine (CysP) forms a sulfenic acid derivative. (IIa) In the resolving step, a second cysteine (CysR) attacks the sulfenic acid to form an inter- or intramolecular disulfide. (IIb) The reaction with an additional peroxide may hyperoxidize CysP to the sulfinic acid form. Hyperoxidation of 2-CysPrx can be retroreduced by the ATP-dependent sulfiredoxin, returning sulfenic forms into the cycle. (III) The regeneration step is catalyzed by a thiol reductant-like NTRC or Trx, reducing the catalytic and resolving cysteine and converting the Prxs to an active thiol peroxidase.

<b>FIG. 3.</b>
FIG. 3.

Role of Prxs in the thiol-dependent redox network. Environmental fluctuations and metabolic disequilibria generate ROS that drain electrons from Prxs that may be considered as redox sensors. Oxidized thiol peroxidases such as Prxs are reduced by redox transmitters, which receive electrons from redox input elements such as NADPH and ferredoxin (Fd). The redox transmitters (Trx, Grx, NTRC, and ACHT) control the redox state of redox targets that act as thiol switches, regulate virtually all cellular processes, and modulate signaling that feeds back to the reducing site and the generator systems. Prxs and ROS may also directly oxidize target proteins by proximity-based oxidation. NTRC, NADPH-dependent thioredoxin reductase C; ROS, reactive oxygen species.

<b>FIG. 4.</b>
FIG. 4.

Multifunctionality of 2-CysPrx in plants. (A) Reduced 2-CysPrx adopts a dimer–decamer equilibrium. Several physicochemical parameters affect this equilibrium: the 2-CysPrx concentration, the pH, and the ionic strength. The critical transition concentration defines the minimum concentration for effective decamer association. Low pH and low ionic strength favor the dimer, whereas high pH and ionic strength support oligomerization. (B) 2-CysPrx is involved in multiple cellular processes based on its redox-dependent conformational state, namely as thiol peroxidase, oxidant of redox transmitters in the redox network, proximity-based oxidase, chaperone, protein interactor, and also as redox indicator in the circadian rhythm.

<b>FIG. 5.</b>
FIG. 5.

Transcripts coexpressed with 2-CysPrx and PrxIIE in Arabidopsis thaliana and Oryza sativa. The correlation coefficients for O. sativa and A. thaliana were obtained from the ATTED-II and the Rice Oligonucleotide Array Database (6, 19). Correlation coefficients were normalized and ranked with 1 for the transcript with maximum level of coregulation and higher numbers according to the position in the list. The query list comprised the Arabidopsis genes with a correlation >0.5. The homologous genes were searched in rice, the degree of coexpression with 2-CysPrx and PrxIIE was determined and plotted against the corresponding coefficient of Arabidopsis. (A) The transcripts in the area with high correlation of >0.5 in both rice and Arabidopsis represent 61% of total analyzed genes, indicating a high level of similarity in coregulation in both species. (C) For PrxIIE, 45% of the selected genes ranged in the area of high coexpression in both species. A selection of interesting genes from this group is given for 2-CysPrx (B) and PrxIIE (D)

<b>FIG. 6.</b>
FIG. 6.

Putative membrane attachment sites of At-2-CysPrx. (A) 2-CysPrx pentadimer with membrane attachment sites highlighted in gray and residing residues shown as stick models. Each subunit contains two membrane attachment sites. The 3D model was constructed with Phyre 2 (

www.sbg.bio.ic.ac.uk/∼phyre

) and PyMOL (29). hPrx2 (PDB ID 1qmv, 62% identity) was used as template (57). (B) 90° turn of 2-CysPrx pentadimer as indicated with viewpoint on the indicated dimer (dotted circle) after rotation. Each monomer is suggested to mediate membrane attachment of one homodimer via two sites (highlighted in gray), the C-terminus and the loop surrounding the substrate entry site. Stick models of residues visible in (A) are not shown in (B) in order to ease the perspective on the lipid peroxide-binding groove (length as dotted line in Ångstrom [Å]). The peroxide-binding groove starts (amino acids counted from the N-terminus) at the positively charged Lys-rich loop near the entrance (aa 35–39), proceeds to the 42ILF44-motif of the β-strand, and ends at the 49DFTFV53 loop close to the CysP (dotted spheres) of the cavity. The resolving Cys of the adjacent monomer is shown as dotted black sphere.

<b>FIG. 7.</b>
FIG. 7.

Assignment of the 2-CysPrx interacting partners to selected metabolic pathways of the chloroplast. The figure is based on diverse findings, in particular, the interactome article by Cerveau et al. (20) and focuses on the photosynthetic electron transport and the associated ferredoxin (Fd), which distributes electron via diverse Fd-dependent proteins to various reductive pathways. The pentagon icon indicates interaction of 2-CysPrx with the proteins. See text for further discussion. ACHT, atypical chloroplast thioredoxin; APR, adenylylsulfate reductase; Cyp20-3, cyclophilin 20-3; γ-ECS, gamma glutamyl cysteine synthase; FBPase, fructose-1,6-bisphosphatase; Fd-GOGAT, ferredoxin-dependent glutamate synthase; FNR, ferredoxin-dependent NADPH reductase; FTR, ferredoxin-dependent thioredoxin reductase; GR, glutathione reductase; IspG, ferredoxin-dependent 4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase; NIR, ferredoxin-dependent nitrite reductase; PC, plastocyanine; PQ, plastoquinone; Psb, photosystem II; PSI/II, photosystem I/II; RubisCO, ribulose-1,5-bisphosphatase; SIR, ferredoxin-dependent sulfite reductase; SOD, superoxide dismutase.

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