Plant chloroplasts generate reactive oxygen species (ROS) during photosynthesis, especially under stresses. The sulfhydryl groups of protein cysteine residues are susceptible to redox modifications, which regulate protein structure and function, and thus different signaling and metabolic processes. The ROS-governed protein thiol redox switches play important roles in chloroplasts.
Recent Advances:
Various high-throughput thiol redox proteomic approaches have been developed, and they have enabled the improved understanding of redox regulatory mechanisms in chloroplasts. For example, the thioredoxin-modulated antioxidant enzymes help to maintain cellular ROS homeostasis. The light- and dark-dependent redox regulation of photosynthetic electron transport, the Calvin/Benson cycle, and starch biosynthesis ensures metabolic coordination and efficient energy utilization. In addition, redox cascades link the light with the dynamic changes of metabolites in nitrate and sulfur assimilation, shikimate pathway, and biosynthesis of fatty acid hormone as well as purine, pyrimidine, and thiamine. Importantly, redox regulation of tetrapyrrole and chlorophyll biosynthesis is critical to balance the photodynamic tetrapyrrole intermediates and prevent oxidative damage. Moreover, redox regulation of diverse elongation factors, chaperones, and kinases plays an important role in the modulation of gene expression, protein conformation, and posttranslational modification that contribute to photosystem II (PSII) repair, state transition, and signaling in chloroplasts.
Critical Issues:
This review focuses on recent advances in plant thiol redox proteomics and redox protein networks toward understanding plant chloroplast signaling, metabolism, and stress responses.
Future Directions:
Using redox proteomics integrated with biochemical and molecular genetic approaches, detailed studies of cysteine residues, their redox states, cross talk with other modifications, and the functional implications will yield a holistic understanding of chloroplast stress responses.
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References
1.
AbatJK and DeswalR. Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of RuBisCO is responsible for the inactivation of its carboxylase activity. Proteomics, 9: 4368–4380, 2009.
2.
AbatJK, MattooAK, and DeswalR. S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata-ribulose-1, 5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J, 275: 2862–2872, 2008.
3.
AkterS, CarpentierS, Van BreusegemF, and MessensJ. Identification of dimedone trapped sulfenylated proteins in plants under stress. Biochem Biophys Rep, 9: 106–113, 2017.
4.
AkterS, HuangJ, BodraN, De SmetB, WahniK, RombautD, PauwelsJ, GevaertK, CarrollK, and Van BreusegemF. DYn-2 based identification of Arabidopsis sulfenomes. Mol Cell Proteomics, 14: 1183–1200, 2015.
5.
AkterS, HuangJ, WaszczakC, JacquesS, GevaertK, Van BreusegemF, and MessensJ. Cysteines under ROS attack in plants: a proteomics view. J Exp Bot, 66: 2935–2944, 2015.
6.
AlivertiA, PiubelliL, ZanettiG, LübberstedtT, HerrmannRG, and CurtiB. The role of cysteine residues of spinach ferredoxin-NADP+ reductase as assessed by site-directed mutagenesis. Biochemistry, 32: 6374–6380, 1993.
7.
AlvarezS, ZhuM, and ChenS. Proteomics of Arabidopsis redox proteins in response to methyl jasmonate. J Proteomics, 73: 30–40, 2009.
8.
AncínM, Fernández-San MillánA, LarrayaL, MoralesF, VeramendiJ, AranjueloI, and FarranI. Overexpression of thioredoxin m in tobacco chloroplasts inhibits the protein kinase STN7 and alters photosynthetic performance. J Exp Bot, 70: 1005–1016, 2018.
9.
AnjoSI, MeloMN, LoureiroLR, SabalaL, CastanheiraP, GrãosM, and ManadasB. oxSWATH: an integrative method for a comprehensive redox-centered analysis combined with a generic differential proteomics screening. Redox Biol, 22: 101130, 2019.
10.
AroEM and OhadI. Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal, 5: 55–67, 2003.
11.
AsadaK.Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol, 141: 391–396, 2006.
12.
BackhausenJE, VetterS, BaalmannE, KitzmannC, and ScheibeR. NAD-dependent malate dehydrogenase and glyceraldehyde 3-phosphate dehydrogenase isoenzymes play an important role in dark metabolism of various plastid types. Planta, 205: 359–366, 1998.
13.
BalmantKM, ParkerJ, YooMJ, ZhuN, DufresneC, and ChenSX. Redox proteomics of tomato in response to Pseudomonas syringae infection. Hortic Res, 2: 15043, 2015.
14.
BalmerY, KollerA, del ValG, ManieriW, SchürmannP, and BuchananBB. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A, 100: 370–375, 2003.
15.
BalmerY, KollerA, ValGD, SchürmannP, and BuchananBB. Proteomics uncovers proteins interacting electrostatically with thioredoxin in chloroplasts. Photosynth Res, 79: 275–280, 2004.
16.
BalmerY, VenselWH, HurkmanWJ, and BuchananBB. Thioredoxin target proteins in chloroplast thylakoid membranes. Antioxid Redox Signal, 8: 1829–1834, 2006.
17.
BeedleAE, LynhamS, and Garcia-ManyesS. Protein S-sulfenylation is a fleeting molecular switch that regulates non-enzymatic oxidative folding. Nat Commun, 7: 12490, 2016.
18.
BerkemeyerM, ScheibeR, and OcheretinaO. A novel, non-redox-regulated NAD-dependent malate dehydrogenase from chloroplasts of Arabidopsis thaliana L. J Biol Chem, 273: 27927–27933, 1998.
19.
BettsSD, RossJR, HallKU, PicherskyE, and YocumCF. Functional reconstitution of photosystem II with recombinant manganese-stabilizing proteins containing mutations that remove the disulfide bridge. Biochim Biophys Acta, 1274: 135–142, 1996.
20.
BhattacharyaS and KumarP. An insilico approach to structural elucidation of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase from Arabidopsis thaliana: hints for herbicide design. Phytochemistry, 73: 7–14, 2012.
BirkenmeierG, StegemannC, HoffmannR, GüntherR, HuseK, and BirkemeyerC. Posttranslational modification of human glyoxalase 1 indicates redox-dependent regulation. PLoS One, 5: e10399, 2012.
23.
BoscoMB, AleanziMC, and IglesiasAÁ. Plastidic phosphoglycerate kinase from Phaeodactylum tricornutum: on the critical role of cysteine residues for the enzyme function. Protist, 163: 188–203, 2012.
24.
BrzezowskiP, RichterAS, and GrimmB. Regulation and function of tetrapyrrole biosynthesis in plants and algae. Biochim Biophys Acta, 1847: 968–985, 2015.
25.
BuchananBB.Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol, 31: 341–374, 1980.
26.
BuchananBB and BalmerY. Redox regulation: a broadening horizon. Annu Rev Plant Biol, 56: 187–220, 2005.
27.
BuchananBB and LuanS. Redox regulation in the chloroplast thylakoid lumen: a new frontier in photosynthesis research. J Exp Bot, 56: 1439–1447, 2005.
28.
BykovaNV and RampitschC. Modulating protein function through reversible oxidation: redox-mediated processes in plants revealed through proteomics. Proteomics, 13: 579–596, 2013.
29.
CarrilloLR, FroehlichJE, CruzJA, SavageL, and KramerDM. Multi-level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance. Plant J, 87: 654–663, 2016.
30.
CejudoFJ, FerrándezJ, CanoB, Puerto-GalánL, and GuineaM. The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling. FEBS Lett, 586: 2974–2980, 2012.
31.
CejudoFJ, MeyerAJ, ReichheldJP, RouhierN, and TraversoJA. Thiol-based redox homeostasis and signaling. Front Plant Sci, 5: 266, 2014.
32.
CerveauD, KrautA, StotzHU, MuellerMJ, CoutéY, and ReyP. Characterization of the Arabidopsis thaliana 2-Cys peroxiredoxin interactome. Plant Sci, 252: 30–41, 2016.
33.
ChangYC, HuangCN, LinCH, ChangHC, and WuCC. Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: an integrated approach to explore the cysteine oxidation. Proteomics, 10: 2961–2971, 2010.
34.
DaQ, WangP, WangM, SunT, JinH, LiuB, WangJ, GrimmB, and WangH-B. Thioredoxin and NADPH-dependent thioredoxin reductase C regulation of tetrapyrrole biosynthesis. Plant Physiol, 175: 652–666, 2017.
35.
De SmetB, WillemsP, Fernandez FernandezAD, AlseekhS, FernieAR, MessensJ, and Van BreusegemF. In vivo detection of protein cysteine sulfenylation in plastids. Plant J, 97: 765–778, 2019.
36.
Del CastelloF, NejamkinA, CassiaR, Correa-AragundeN, FernándezB, ForesiN, LombardoC, RamirezL, and LamattinaL. The era of nitric oxide in plant biology: twenty years tying up loose ends. Nitric Oxide, 85: 17–27, 2019.
37.
DepègeN, BellafioreS, and RochaixJD. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science, 299: 1572–1575, 2003.
38.
DietzK-J.Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal, 15: 1129–1159, 2011.
39.
DietzK-J.Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast?. Mol Cells, 39: 20–25, 2016.
40.
DietzelL, BräutigamK, and PfannschmidtT. Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry–functional relationships between short-term and long-term light quality acclimation in plants. FEBS J, 275: 1080–1088, 2008.
41.
DixonDP, DavisBG, and EdwardsR. Functional divergence in the glutathione transferase superfamily in plants: identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem, 277: 30859–30869, 2002.
42.
DixonDP, SkipseyM, GrundyNM, and EdwardsR. Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol, 138: 2233–2244, 2005.
43.
DograV, RochaixJD, and KimC. Singlet oxygen-triggered chloroplast-to-nucleus retrograde signalling pathways: an emerging perspective. Plant Cell Environ, 41: 1727–1738, 2018.
44.
Dominguez-SolisJR, HeZ, LimaA, TingJ, BuchananBB, and LuanS. A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc Natl Acad Sci U S A, 105: 16386–16391, 2008.
45.
DumasL, ZitoF, BlangyS, AuroyP, and AlricJ. A stromal region of cytochrome b6f subunit IV is involved in the activation of the Stt7 kinase in Chlamydomonas. Proc Natl Acad Sci U S A, 114: 12063–12068, 2017.
46.
EjimaK, KawaharadaT, InoueS, KojimaK, and NishiyamaY. A change in the sensitivity of elongation factor G to oxidation protects photosystem II from photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett, 586: 778–783, 2012.
47.
EntusR, PolingM, and HerrmannKM. Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase. Plant Physiol, 129: 1866–1871, 2002.
48.
FengJ, ChenL, and ZuoJ. Protein S-nitrosylation in plants: current progresses and challenges. J Integr Plant Biol, 61: 1206–1223, 2019.
49.
FlorencioFJ, GadalP, and BuchananBB. Thioredoxin-linked activation of the chloroplast and cytosolic forms of Chlamydomonas reinhardtii glutamine synthetase. Plant Physiol Biochem, 31: 649–655, 1993.
50.
GalantA, KoesterRP, AinsworthEA, HicksLM, and JezJM. From climate change to molecular response: redox proteomics of ozone-induced responses in soybean. New Phytol, 194: 220–229, 2012.
51.
García-MurriaMJ, SudhaniHPK, Marín-NavarroJ, Sánchez Del PinoMM, and MorenoJ. Dissecting the individual contribution of conserved cysteines to the redox regulation of RubisCO. Photosynth Res, 137: 251–262, 2018.
52.
GietlerM, NykielM, OrzechowskiS, FettkeJ, and ZagdańskaB. Proteomic analysis of S-nitrosylated and S-glutathionylated proteins in wheat seedlings with different dehydration tolerances. Plant Physiol Biochem, 108: 507–518, 2016.
53.
GiudiceAD, PavelNV, GalantiniL, FaliniG, TrostP, FermaniS, and SparlaF. Unravelling the shape and structural assembly of the photosynthetic GAPDH-CP12-PRK complex from Arabidopsis thaliana by small-angle X-ray scattering analysis. Acta Crystallogr, 71: 2372–2385, 2015.
54.
GlaringMA, SkryhanK, KöttingO, ZeemanSC, and BlennowA. Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol Biochem, 58: 89–97, 2012.
55.
GromesR, HothornM, LenherrED, RybinV, ScheffzekK, and RauschT. The redox switch of γ-glutamylcysteine ligase via a reversible monomer–dimer transition is a mechanism unique to plants. Plant J, 54: 1063–1075, 2008.
56.
GütleDD, RoretT, HeckerA, ReskiR, and JacquotJ-P. Dithiol disulphide exchange in redox regulation of chloroplast enzymes in response to evolutionary and structural constraints. Plant Sci, 255: 1–11, 2017.
57.
HädrichN, HendriksJH, KöttingO, ArrivaultS, FeilR, ZeemanSC, GibonY, SchulzeWX, StittM, and LunnJE. Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J, 70: 231–242, 2012.
58.
HallM, Mata-CabanaA, ÅkerlundHE, FlorencioFJ, SchröderWP, LindahlM, and KieselbachT. Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function. Proteomics, 10: 987–1001, 2010.
59.
HeY, MawhinneyTP, PreussML, SchroederAC, ChenB, AbrahamL, JezJM, and ChenS. A redox-active isopropylmalate dehydrogenase functions in the biosynthesis of glucosinolates and leucine in Arabidopsis. Plant J, 60: 679–690, 2009.
60.
HendriksJH, KolbeA, GibonY, StittM, and GeigenbergerP. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol, 133: 838–849, 2003.
61.
Herrera-VásquezA, SalinasP, and HoluigueL. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci, 6: 171, 2015.
62.
HicksLM, CahoonRE, BonnerER, RivardRS, SheffieldJ, and JezJM. Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell, 19: 2653–2661, 2007.
63.
HisaboriT, SunamuraE-I, KimY, and KonnoH. The chloroplast ATP synthase features the characteristic redox regulation machinery. Antioxid Redox Signal, 19: 1846–1854, 2013.
HuangD, HuoJ, ZhangJ, WangC, WangB, FangH, and LiaoW. Protein S-nitrosylation in programmed cell death in plants. Cell Mol Life Sci, 76: 1877–1887, 2019.
66.
ItoH, IwabuchiM, and OgawaKi. The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol, 44: 655–660, 2003.
67.
JimboH, YutthanasirikulR, NaganoT, HisaboriT, HiharaY, and NishiyamaY. Oxidation of translation factor EF-Tu inhibits the repair of photosystem II. Plant Physiol, 176: 2691–2699, 2018.
68.
KamedaH, HirabayashiK, WadaK, and FukuyamaK. Mapping of protein-protein interaction sites in the plant-type [2Fe-2S] ferredoxin. PLoS One, 6: e21947, 2011.
69.
KangZH and WangGX. Redox regulation in the thylakoid lumen. J Plant Physiol, 192: 28–37, 2016.
70.
KaramokoM, ClineS, ReddingK, RuizN, and HamelPP. Lumen thiol oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis. Plant Cell, 23: 4462–4475, 2011.
71.
KatoH, TakemotoD, and KawakitaK. Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant, 148: 371–386, 2013.
72.
KitajimaS.Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-Cys peroxiredoxin. Photochem Photobiol, 84: 1404–1409, 2008.
73.
KitajimaS, KuriokaM, YoshimotoT, ShindoM, KanaoriK, TajimaK, and OdaK. A cysteine residue near the propionate side chain of heme is the radical site in ascorbate peroxidase. FEBS J, 275: 470–480, 2008.
74.
KojimaK, MotohashiK, MorotaT, OshitaM, HisaboriT, HayashiH, and NishiyamaY. Regulation of translation by the redox state of elongation factor G in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem, 284: 18685–18691, 2009.
75.
KojimaK, OshitaM, NanjoY, KasaiK, TozawaY, HayashiH, and NishiyamaY. Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol, 65: 936–947, 2007.
76.
KozakiA, MayumiK, and SasakiY. Thiol-disulfide exchange between nuclear-encoded and chloroplast-encoded subunits of pea acetyl-CoA carboxylase. J Biol Chem, 276: 39919–39925, 2001.
77.
LangenkämperG, Manac'HN, BroinM, CuinéS, BecuweN, KuntzM, and ReyP. Accumulation of plastid lipid-associated proteins (fibrillin/CDSP34) upon oxidative stress, ageing and biotic stress in Solanaceae and in response to drought in other species. J Exp Bot, 52: 1545–1554, 2001.
78.
LaureM, MirkoZ, SamuelM, FrancescaS, EstherPPM, FrancescoF, AntoineD, MarchandCH, SimonaF, and PaoloT. Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci, 4: 470, 2013.
79.
LaxaM, KönigJ, DietzK-J, and KandlbinderA. Role of the cysteine residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis–trans isomerase and redox-related functions. Biochem J, 401: 287–297, 2007.
80.
LeeES, KangCH, ParkJH, and LeeSY. Physiological significance of plant peroxiredoxins (Prxs) and the structure-related and multi-functional biochemistry of Prx1. Antioxid Redox Signal, 28: 625–639, 2018.
81.
LemaireSD, GuillonB, LeMP, KeryerE, Miginiac-MaslowM, and DecottigniesP. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A, 101: 7475–7480, 2004.
82.
LemeilleS, and RochaixJ-D. State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res, 106: 33–46, 2010.
83.
LepistöA, PakulaE, ToivolaJ, Krieger LiszkayA, VignolsF, and RintamäkiE. Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods. J Exp Bot, 64: 3843–3854, 2013.
84.
LiM, YangQ, ZhangL, HanL, CuiY, and WuQ. Identification of novel targets of cyanobacterial glutaredoxin. Arch Biochem Biophys, 458: 220–228, 2007.
85.
LiY, LiuB, ZhangJ, KongF, ZhangL, MengH, LiW, RochaixJ-D, LiD, and PengL. OHP1, OHP2, and HCF244 form a transient functional complex with the photosystem II reaction center. Plant Physiol, 179: 195–208, 2019.
86.
LichterA and HäberleinI. A light-dependent redox signal participates in the regulation of ammonia fixation in chloroplasts of higher plants—ferredoxin: glutamate synthase is a thioredoxin-dependent enzyme. J Plant Physiol, 153: 83–90, 1998.
87.
LinA, WangY, TangJ, XueP, LiC, LiuL, HuB, YangF, LoakeGJ, and ChuC. Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol, 158: 451–464, 2012.
88.
LindC, GerdesR, HamnellY, Schuppe-KoistinenI, von LöwenhielmHB, HolmgrenA, and CotgreaveIA. Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch Biochem Biophys, 406: 229–240, 2002.
89.
LindahlM and FlorencioFJ. Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci U S A, 100: 16107–16112, 2003.
90.
LindahlM and KieselbachT. Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria. J Proteomics, 72: 416–438, 2009.
91.
LindahlM, Mata CabanaA, and KieselbachT. The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal, 14: 2581–2642, 2011.
92.
LindermayrC, SaalbachG, and DurnerJ. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol, 137: 921–930, 2005.
93.
LiuP, ZhangH, WangH, and XiaY. Identification of redox-sensitive cysteines in the Arabidopsis proteome using OxiTRAQ, a quantitative redox proteomics method. Proteomics, 14: 750–762, 2014.
94.
LiuP, ZhangH, YuB, XiongL, and XiaY. Proteomic identification of early salicylate-and flg22-responsive redox-sensitive proteins in Arabidopsis. Sci Rep, 5: 8625, 2015.
95.
Lo Conte M and CarrollKS.Chemoselective ligation of sulfinic acids with aryl-nitroso compounds. Angew Chem, 124: 6608–6611, 2012.
96.
LowtherWT and HaynesAC. Reduction of cysteine sulfinic acid in eukaryotic, typical 2-Cys peroxiredoxins by sulfiredoxin. Antioxid Redox Signal, 15: 99–109, 2011.
97.
LuoT, FanT, LiuY, RothbartM, YuJ, ZhouS, GrimmB, and LuoM. Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants. Plant Physiol, 159: 118–130, 2012.
98.
MaedaH and DudarevaN. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol, 63: 73–105, 2012.
99.
MarchandC, Le MaréchalP, MeyerY, and DecottigniesP. Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics, 6: 6528–6537, 2006.
100.
MarchandC, Le MaréchalP, MeyerY, Miginiac-MaslowM, Issakidis-BourguetE, and DecottigniesP. New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics, 4: 2696–2706, 2004.
101.
MarriL, ZaffagniniM, CollinV, Issakidis-BourguetE, LemaireSD, PupilloP, SparlaF, Miginiac-MaslowM, and TrostP. Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Mol Plant, 2: 259–269, 2009.
102.
Mata-CabanaA, FlorencioFJ, and LindahlM. Membrane proteins from the cyanobacterium Synechocystis sp. PCC 6803 interacting with thioredoxin. Proteomics, 7: 3953–3963, 2007.
103.
MeyerY, BelinC, Delorme-HinouxV, ReichheldJP, and RiondetC. Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal, 17: 1124–1160, 2012.
104.
MichalskaJ, ZauberH, BuchananBB, CejudoFJ, and GeigenbergerP. NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci U S A, 106: 9908–9913, 2009.
105.
MicheletL, ZaffagniniM, VanackerH, MarechalPL, MarchandC, SchrodaM, LemaireSD, and DecottigniesP. In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J Biol Chem, 283: 21571–21578, 2008.
106.
MikkelsenR, MutendaKE, MantA, SchürmannP, and BlennowA. Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci U S A, 102: 1785–1790, 2005.
107.
MommaM and FujimotoZ. Interdomain disulfide bridge in the rice granule bound starch synthase I catalytic domain as elucidated by X-ray structure analysis. Biosci Biotechnol Biochem, 76: 1591–1595, 2012.
108.
MontrichardF, AlkhalfiouiF, YanoH, VenselWH, HurkmanWJ, and BuchananBB. Thioredoxin targets in plants: the first 30 years. J Proteomics, 72: 452–474, 2009.
109.
MoonH, LeeB, ChoiG, ShinD, PrasadDT, LeeO, KwakS-S, KimDH, NamJ, BahkJ, HongJC, LeeSY, ChoMJ, LimCO, and YunDJ. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci U S A, 100: 358–363, 2003.
110.
MorenoJ, GarcíamurriaMJ, and MarínnavarroJ. Redox modulation of RubisCO conformation and activity through its cysteine residues. J Exp Bot, 59: 1605–1614, 2008.
111.
MorisseS, MicheletL, BedhommeM, MarchandCH, CalvaresiM, TrostP, FermaniS, ZaffagniniM, and LemaireSD. Thioredoxin-dependent redox regulation of chloroplastic phosphoglycerate kinase from Chlamydomonas reinhardtii. J Biol Chem, 289: 30012–30024, 2014.
112.
MotohashiK and HisaboriT. HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem, 281: 35039–35047, 2006.
113.
MotohashiK, KondohA, StumppMT, and HisaboriT. Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci U S A, 98: 11224–11229, 2001.
114.
MotohashiK, KoyamaF, NakanishiY, UeokanakanishiH, and HisaboriT. Chloroplast cyclophilin is a target protein of thioredoxin. J Biol Chem, 278: 31848–31852, 2003.
115.
MouZ, FanW, and DongX. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113: 935–944, 2003.
116.
MurakamiR, IfukuK, TakabayashiA, ShikanaiT, EndoT, and SatoF. Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2. FEBS J, 272: 2165–2175, 2005.
117.
MuthuramalingamM, MatrosA, ScheibeR, MockH-P, and DietzK-J. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Front Plant Sci, 4: 54, 2013.
118.
NakaoLS, EverleyRA, MarinoSM, LoSM, de SouzaLE, GygiSP, and GladyshevVN. Mechanism-based proteomic screening identifies targets of thioredoxin-like proteins. J Biol Chem, 290: 5685–5695, 2015.
119.
NikitinaJ, ShutovaT, MelnikB, ChernyshovS, MarchenkovV, SemisotnovG, KlimovV, and SamuelssonG. Importance of a single disulfide bond for the PsbO protein of photosystem II: protein structure stability and soluble overexpression in Escherichia coli. Photosynth Res, 98: 391, 2008.
120.
NikkanenL, Guinea DiazM, ToivolaJ, TiwariA, and RintamäkiE. Multilevel regulation of non-photochemical quenching and state transitions by chloroplast NADPH-dependent thioredoxin reductase. Physiol Plant, 166: 211–225, 2019.
121.
NikkanenL, ToivolaJ, and RintamäkiE. Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis. Plant Cell Environ, 39: 1691–1705, 2016.
122.
NishiyamaY, YamamotoH, AllakhverdievSI, InabaM, YokotaA, and MurataN. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J, 20: 5587–5594, 2001.
123.
Ortega-GalisteoAP, Rodríguez-SerranoM, PazmiñoDM, GuptaDK, SandalioLM, and Romero-PuertasMC. S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot, 63: 2089–2103, 2012.
124.
PaoloP, AlexanderH, MathiasP, AnjaS, TatjanaK, and DarioL. Optimizing photosynthesis under fluctuating light: the role of the Arabidopsis STN7 kinase. Plant Signal Behav, 5: 21–25, 2010.
125.
ParkSW, LiW, ViehhauserA, HeB, KimS, NilssonAK, AnderssonMX, KittleJD, AmbavaramMM, and LuanS. Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc Natl Acad Sci U S A, 110: 9559–9564, 2013.
126.
ParkerJ, BalmantK, ZhuF, ZhuN, and ChenS. cysTMTRAQ—an integrative method for unbiased thiol-based redox proteomics. Mol Cell Proteomics, 14: 237–242, 2015.
127.
Pérez-PérezME, FlorencioFJ, and LindahlM. Selecting thioredoxins for disulphide proteomics: target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803. Proteomics, 6: 186–195, 2006.
128.
Pérez-RuizJM and CejudoFJ. A proposed reaction mechanism for rice NADPH thioredoxin reductase C, an enzyme with protein disulfide reductase activity. FEBS Lett, 583: 1399–1402, 2009.
129.
Pérez-RuizJM, NaranjoB, OjedaV, GuineaM, and CejudoFJ. NTRC-dependent redox balance of 2-Cys peroxiredoxins is needed for optimal function of the photosynthetic apparatus. Proc Natl Acad Sci U S A, 114: 12069–12074, 2017.
130.
This reference has been deleted.
131.
Pérez-RuizJM, GuineaM, PuertogalánL, and CejudoFJ. NADPH thioredoxin reductase C is involved in redox regulation of the Mg-chelatase I subunit in Arabidopsis thaliana chloroplasts. Mol Plant, 7: 1252–1255, 2014.
132.
PortisAR, LiC, WangD, and SalvucciME. Regulation of RubisCO activase and its interaction with RubisCO. J Exp Bot, 59: 1597–1604, 2007.
133.
Puerto-GalánL, Pérez-RuizJM, FerrándezJ, CanoB, NaranjoB, NájeraVA, GonzálezM, LindahlAM, and CejudoFJ. Overoxidation of chloroplast 2-Cys peroxiredoxins: balancing toxic and signaling activities of hydrogen peroxide. Front Plant Sci, 4: 310, 2013.
134.
PuthiyaveetilS.A mechanism for regulation of chloroplast LHC II kinase by plastoquinol and thioredoxin. FEBS Lett, 585: 1717–1721, 2011.
135.
PuyaubertJ, FaresA, RézéN, PeltierJ-B, and BaudouinE. Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci, 215: 150–156, 2014.
136.
ReyP, CuinéS, EymeryF, GarinJ, CourtM, JacquotJP, RouhierN, and BroinM. Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J, 41: 31–42, 2005.
137.
RichterAS and BernhardG. Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway in plants. Front Plant Sci, 4: 2636–2646, 2013.
138.
RichterAS, PeterE, RothbartM, SchlickeH, ToivolaJ, RintamäkiE, and GrimmB. Posttranslational influence of NTRC on enzymes in tetrapyrrole synthesis. Plant Physiol, 162: 63–73, 2013.
139.
RintamäkiE, MartinsuoP, PursiheimoS, and AroEM. Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci U S A, 97: 11644–11649, 2000.
140.
RitteG, HeydenreichM, MahlowS, HaebelS, KöttingO, and SteupM. Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett, 580: 4872–4876, 2006.
141.
RobertsIN, LamXT, MirandaH, KieselbachT, and FunkC. Degradation of PsbO by the Deg protease HhoA is thioredoxin dependent. PLoS One, 7: e45713, 2012.
142.
Romero-PuertasMC, CampostriniN, MattèA, RighettiPG, PerazzolliM, ZollaL, RoepstorffP, and DelledonneM. Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics, 8: 1459–1469, 2008.
143.
RomeropuertasMC, LaxaM, MattèA, ZaninottoF, FinkemeierI, JonesAME, PerazzolliM, VandelleE, DietzKJ, and DelledonneM. S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell, 19: 4120–4130, 2008.
SasakiY, KozakiA, and HatanoM. Link between light and fatty acid synthesis: thioredoxin-linked reductive activation of plastidic acetyl-CoA carboxylase. Proc Natl Acad Sci U S A, 94: 11096–11101, 1997.
146.
ScheibeR.Malate valves to balance cellular energy supply. Physiol Plant, 120: 21–26, 2004.
147.
SchürmannP and BuchananBB. The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal, 10: 1235–1274, 2008.
148.
SerratoAJ, Fernández TrijuequeJ, Barajas LópezJDD, ChuecaA, and SahrawyM. Plastid thioredoxins: a “one-for-all” redox-signaling system in plants. Front Plant Sci, 4: 463, 2013.
149.
SerratoAJ, PérezruizJM, SpínolaMC, and CejudoFJ. A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem, 279: 43821–43827, 2004.
150.
ShapiguzovA, ChaiX, FucileG, LongoniP, ZhangL, and RochaixJ-D. Activation of the Stt7/STN7 kinase through dynamic interactions with the cytochrome b6f complex. Plant Physiol, 171: 82–92, 2016.
151.
SimionatoD, BassoS, ZaffagniniM, LanaT, MarzottoF, TrostP, and MorosinottoT. Protein redox regulation in the thylakoid lumen: the importance of disulfide bonds for violaxanthin de-epoxidase. FEBS Lett, 589: 919–923, 2015.
152.
SkryhanK, GurrieriL, SparlaF, TrostP, and BlennowA. Redox regulation of starch metabolism. Front Plant Sci, 9: 1344, 2018.
153.
SmithAG, SantanaMA, WallacecookAD, RoperJM, and LabbeboisR. Isolation of a cDNA encoding chloroplast ferrochelatase from Arabidopsis thaliana by functional complementation of a yeast mutant. J Biol Chem, 269: 13405–13413, 1994.
154.
SparlaF, PupilloP, and TrostP. The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem, 277: 44946–44952, 2002.
155.
SparlaF, ZaffagniniM, WedelN, ScheibeR, PupilloP, and TrostP. Regulation of photosynthetic GAPDH dissected by mutants. Plant Physiol, 138: 2210–2219, 2005.
156.
StanleyDN, RainesCA, and KerfeldCA. Comparative analysis of 126 cyanobacterial genomes reveals evidence of functional diversity among homologs of the redox-regulated CP12 protein. Plant Physiol, 161: 824–835, 2013.
157.
StröherE and DietzKJ. The dynamic thiol-disulphide redox proteome of the Arabidopsis thaliana chloroplast as revealed by differential electrophoretic mobility. Physiol Plant, 133: 566–583, 2008.
158.
TanouG, JobC, RajjouL, ArcE, BelghaziM, DiamantidisG, MolassiotisA, and JobD. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J, 60: 795–804, 2009.
159.
TiessenA, HendriksJH, StittM, BranscheidA, GibonY, FarréEM, and GeigenbergerP. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell, 14: 2191–2213, 2002.
160.
TossounianMA, VanMI, WahniK, JacquesS, GevaertK, VanBF, VertommenD, YoungD, RosadoLA, and MessensJ. Disulfide bond formation protects Arabidopsis thaliana glutathione transferase tau 23 from oxidative damage. Biochim Biophys Acta, 1862: 775–789, 2018.
161.
TrostP, FermaniS, MarriL, ZaffagniniM, FaliniG, ScagliariniS, PupilloP, and SparlaF. Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms. Photosynth Res, 89: 263–275, 2006.
162.
TsukamotoY, FukushimaY, HaraS, and HisaboriT. Redox control of the activity of phosphoglycerate kinase in Synechocystis sp. PCC6803. Plant Cell Physiol, 54: 484–491, 2013.
163.
TuncozdemirM, MillerG, SongL, KimJ, SodekA, KoussevitzkyS, MisraAN, MittlerR, and ShintaniD. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol, 151: 421–432, 2009.
164.
TytherR, AhmedaA, JohnsE, McDonaghB, and SheehanD. Proteomic profiling of perturbed protein sulfenation in renal medulla of the spontaneously hypertensive rat. J Proteome Res, 9: 2678–2687, 2010.
165.
UpchurchRG.Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett, 30: 967–977, 2008.
166.
VajrychovaM, SalovskaB, PimkovaK, FabrikI, TamborV, KondelovaA, BartekJ, and HodnyZ. Quantification of cellular protein and redox imbalance using SILAC-iodoTMT methodology. Redox Biol, 24: 101227, 2019.
167.
VieiraDSC and ReyP. Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci, 11: 329–334, 2006.
168.
VossI, KoelmannM, WojteraJ, HoltgrefeS, KitzmannC, BackhausenJE, and ScheibeR. Knockout of major leaf ferredoxin reveals new redox-regulatory adaptations in Arabidopsis thaliana. Physiol Plant, 133: 584–598, 2008.
169.
WangH, WangS, LuY, AlvarezS, HicksLM, GeX, and XiaY. Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis. J Proteome Res, 11: 412–424, 2012.
170.
WangW, VinocurB, ShoseyovO, and AltmanA. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci, 9: 244–252, 2004.
171.
WaszczakC, AkterS, EeckhoutD, PersiauG, WahniK, BodraN, Van MolleI, De SmetB, VertommenD, and GevaertK. Sulfenome mining in Arabidopsis thaliana. Proc Natl Acad Sci U S A, 111: 11545–11550, 2014.
172.
WaszczakC, CarmodyM, and KangasjärviJ. Reactive oxygen species in plant signaling. Annu Rev Plant Biol, 69: 209–236, 2018.
173.
WuG and OrtDR. Mutation in the cysteine bridge domain of the gamma-subunit affects light regulation of the ATP synthase but not photosynthesis or growth in Arabidopsis. Photosynth Res, 97: 185–193, 2008.
174.
WymanAJ and YocumCF. Structure and activity of the photosystem II manganese-stabilizing protein: role of the conserved disulfide bond. Photosynth Res, 85: 359–372, 2005.
175.
XuY and NeelB.Activated thiol sepharose-based proteomic approach to globally quantify protein oxidation. bioRxiv 549709, 2019.
176.
YamazakiD, MotohashiK, KasamaT, HaraY, and HisaboriT. Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol, 45: 18–27, 2004.
177.
YangJ, CarrollKS, and LieblerDC. The expanding landscape of the thiol redox proteome. Mol Cell Proteomics, 15: 1–11, 2016.
178.
YangJ, GuptaV, TallmanKA, PorterNA, CarrollKS, and LieblerDC. Global, in situ, site-specific analysis of protein S-sulfenylation. Nat Protoc, 10: 1022–1037, 2015.
179.
YanoH, WongJH, LeeYM, ChoM-J, and BuchananBB. A strategy for the identification of proteins targeted by thioredoxin. Proc Natl Acad Sci U S A, 98: 4794–4799, 2001.
180.
YinZ, BalmantK, GengS, ZhuN, ZhangT, DufresneC, DaiS, and ChenS. Bicarbonate induced redox proteome changes in Arabidopsis suspension cells. Front Plant Sci, 8: 58, 2017.
181.
YoshidaK, HaraA, SugiuraK, FukayaY, and HisaboriT. Thioredoxin-like2/2-Cys peroxiredoxin redox cascade supports oxidative thiol modulation in chloroplasts. Proc Natl Acad Sci U S A, 115: 8296–8304, 2018.
182.
YoshidaK and HisaboriT. Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability. Proc Natl Acad Sci U S A, 113: 3967–3976, 2016.
183.
YuQB, MaQ, KongMM, ZhaoTT, ZhangXL, ZhouQ, HuangC, ChongK, and YangZN. AtECB1/MRL7, a thioredoxin-like fold protein with disulfide reductase activity, regulates chloroplast gene expression and chloroplast biogenesis in Arabidopsis thaliana. Mol Plant, 7: 206–217, 2014.
184.
YuQB, ZhaoTT, YeLS, ChengL, WuYQ, HuangC, and YangZN. pTAC10, an S1-domain-containing component of the transcriptionally active chromosome complex, is essential for plastid gene expression in Arabidopsis thaliana and is phosphorylated by chloroplast-targeted casein kinase II. Photosynth Res, 137: 69–83, 2018.
185.
YutthanasirikulR, NaganoT, JimboH, HiharaY, KanamoriT, UedaT, HaruyamaT, KonnoH, YoshidaK, and HisaboriT. Oxidation of a cysteine residue in elongation factor EF-Tu reversibly inhibits translation in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem, 291: 5860–5870, 2016.
186.
ZaffagniniM, BedhommeM, GroniH, MarchandCH, PuppoC, GonteroB, Cassier-ChauvatC, DecottigniesP, and LemaireSD. Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol Cell Proteomics, 11: M111.014142, 2012.
187.
ZaffagniniM, FermaniS, MarchandCH, CostaA, SparlaF, RouhierN, GeigenbergerP, LemaireSD, and TrostP. Redox homeostasis in photosynthetic organisms: novel and established thiol-based molecular mechanisms. Antioxid Redox Signal, 31: 155–210, 2018.
188.
ZaffagniniM, MicheletL, MarchandC, SparlaF, DecottigniesP, LeMP, MiginiacmaslowM, NoctorG, TrostP, and LemaireSD. The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J, 274: 212–226, 2007.
189.
ZhangL, PuH, DuanZ, LiY, LiuB, ZhangQ, LiW, RochaixJD, LiuL, and PengL. Nucleus-encoded protein BFA1 promotes efficient assembly of the chloroplast ATP synthase coupling factor 1. Plant Cell, 30: 1770–1788, 2018.
190.
ZhangN and PortisAR. Mechanism of light regulation of RubisCO: a specific role for the larger RubisCO activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci U S A, 96: 9438–9443, 1999.
191.
ZhangN, SchürmannP, and PortisARJr. Characterization of the regulatory function of the 46-kDa isoform of RubisCO activase from Arabidopsis. Photosynth Res, 68: 29–37, 2001.
192.
ZhangT, ZhuM, ZhuN, StrulJM, DufresneCP, SchneiderJD, HarmonAC, and ChenS. Identification of thioredoxin targets in guard cell enriched epidermal peels using cysTMT proteomics. J Proteomics, 133: 48–53, 2016.
193.
ZhuM, ZhuN, SongWY, HarmonAC, AssmannSM, and ChenS. Thiol-based redox proteins in abscisic acid and methyl jasmonate signaling in Brassica napus guard cells. Plant J, 78: 491–515, 2014.
194.
ZouY, WangA, ShiM, ChenX, LiuR, LiT, ZhangC, ZhangZ, ZhuL, and JuZ. Analysis of redox landscapes and dynamics in living cells and in vivo using genetically encoded fluorescent sensors. Nat Protoc, 13: 2362–2386, 2018.
195.
ZrennerR, StittM, SonnewaldU, and BoldtR. Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol, 57: 805–836, 2005.
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