Arabidopsis dehydroascorbate reductase 1 and 2 modulate redox states of ascorbate-glutathione cycle in the cytosol in response to photooxidative stress

References

• Chen M, Chory J, Fankhauser C. Light signal transduction in higher plants. Annu Rev Genet. 2004;38:87–117.10.1146/annurev.genet.38.072902.092259
   PubMed Web of Science ®Google Scholar
• Jiao Y, Lau OS, Deng XW. Light-regulated transcriptional networks in higher plants. Nat Rev Genet. 2007;8:217–230.10.1038/nrg2049
   PubMed Web of Science ®Google Scholar
• Eberhard S, Finazzi G, Wollman FA. The dynamics of photosynthesis. Annu Rev Genet. 2008;42:463–515.10.1146/annurev.genet.42.110807.091452
   PubMed Web of Science ®Google Scholar
• Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant. 2003;119:355–364.10.1034/j.1399-3054.2003.00223.x
   Web of Science ®Google Scholar
• Mittler R, Vanderauwera S, Gollery M, et al. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498.10.1016/j.tplants.2004.08.009
   PubMed Web of Science ®Google Scholar
• Gadjev I, Vanderauwera S, Gechev TS, et al. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 2006;141:436–445.10.1104/pp.106.078717
   PubMed Web of Science ®Google Scholar
• Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011;155:93–100.10.1104/pp.110.166181
   PubMed Web of Science ®Google Scholar
• Schmidt R, Schippers JH. ROS-mediated redox signaling during cell differentiation in plants. Biochem Biophys Acta. 2014;1850:1497–1508.
   PubMed Web of Science ®Google Scholar
• Foyer CH, Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 2011;155:2–18.10.1104/pp.110.167569
   PubMed Web of Science ®Google Scholar
• Asada K. The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:601–639.10.1146/annurev.arplant.50.1.601
   PubMed Web of Science ®Google Scholar
• Shigeoka S, Ishikawa T, Tamoi M, et al. Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot. 2002;53:1305–1319.10.1093/jexbot/53.372.1305
   PubMed Web of Science ®Google Scholar
• Chew O, Whelan J, Millar AH. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem. 2003;278:46869–46877.10.1074/jbc.M307525200
   PubMed Web of Science ®Google Scholar
• Gallie DR. The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot. 2013;64:433–443.10.1093/jxb/ers330
   PubMed Web of Science ®Google Scholar
• Shigeoka S, Maruta T. Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem. 2014;78:1457–1470.10.1080/09168451.2014.942254
   PubMed Web of Science ®Google Scholar
• Munné-Bosch S, Alegre L. Interplay between ascorbic acid and lipophilic antioxidant defences in chloroplasts of water-stressed Arabidopsis plants. FEBS Lett. 2002;524:145–148.10.1016/S0014-5793(02)03041-7
   PubMed Web of Science ®Google Scholar
• Szarka A, Tomasskovics B, Bánhegyi G. The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int J Mol Sci. 2012;13:4458–4483.10.3390/ijms13044458
   PubMed Web of Science ®Google Scholar
• Niyogi KK. Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Mol Biol. 1999;50:333–359.10.1146/annurev.arplant.50.1.333
   PubMed Web of Science ®Google Scholar
• Smirnoff N, Wheeler GL. Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol. 2000;35:291–314.10.1080/10409230008984166
   PubMed Web of Science ®Google Scholar
• Muller-Moule P, Conklin PL, Niyogi KK. Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol. 2002;128:970–977.10.1104/pp.010924
   PubMed Web of Science ®Google Scholar
• Mano J, Hideg E, Asada K. Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys. 2004;429:71–80.10.1016/j.abb.2004.05.022
   PubMed Web of Science ®Google Scholar
• Tóth SZ, Schansker G, Garab G. The physiological roles and metabolism of ascorbate in chloroplasts. Physiol Plant. 2013;148:161–175.10.1111/ppl.2013.148.issue-2
   PubMed Web of Science ®Google Scholar
• Chen Z, Young TE, Ling J, et al. Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA. 2003;100:3525–3530.10.1073/pnas.0635176100
   PubMed Web of Science ®Google Scholar
• Chen Z, Gallie DR. Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol. 2006;142:775–787.10.1104/pp.106.085506
   PubMed Web of Science ®Google Scholar
• Chen Z, Gallie DR. Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance. J Biol Chem. 2008;283:21347–21361.10.1074/jbc.M802601200
   PubMed Web of Science ®Google Scholar
• Chen Z, Gallie DR. The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell. 2004;16:1143–1162.10.1105/tpc.021584
   PubMed Web of Science ®Google Scholar
• Dixon DP, Edwards R. Glutathione transferases. Arabidopsis Book. 2010;8:e0131.10.1199/tab.0131
   PubMedGoogle Scholar
• Noshi M, Hatanaka R, Tanabe N, et al. Redox regulation of ascorbate and glutathione by a chloroplastic dehydroascorbate reductase is required for high-light stress tolerance in Arabidopsis. Biosci Biotechnol Biochem. 2016;80:870–877.10.1080/09168451.2015.1135042
   PubMed Web of Science ®Google Scholar
• Yoshida S, Tamaoki M, Shikano T, et al. Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol. 2006;47:304–308.
   PubMed Web of Science ®Google Scholar
• Reumann S, Quan S, Aung K, et al. In-depth proteome analysis of arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol. 2009;150:125–143.10.1104/pp.109.137703
   PubMed Web of Science ®Google Scholar
• Grefen C, Donald N, Hashimoto K, et al. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 2010;64:355–365.10.1111/tpj.2010.64.issue-2
   PubMed Web of Science ®Google Scholar
• Wang Z, Xiao Y, Chen W, et al. Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol. 2010;52:400–409.10.1111/jipb.2010.52.issue-4
   PubMed Web of Science ®Google Scholar
• Vadassery J, Tripathi S, Prasad R, et al. Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol. 2009;166:1263–1274.10.1016/j.jplph.2008.12.016
   PubMed Web of Science ®Google Scholar
• Shigeoka S, Nakano Y, Kitaoka S. Metabolism of hydrogen peroxide in Euglena gracilis z by L-ascorbic acid peroxidase. Biochem J. 1980;186:377–380.10.1042/bj1860377
   PubMed Web of Science ®Google Scholar
• Eltayeb AE, Kawano N, Badawi GH, et al. Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta. 2007;225:1255–1264.10.1007/s00425-006-0417-7
   PubMed Web of Science ®Google Scholar
• Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta. 1976;133:21–25.10.1007/BF00386001
   PubMed Web of Science ®Google Scholar
• Maruta T, Noshi M, Tanouchi A, et al. H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem. 2012;287:11717–11729.10.1074/jbc.M111.292847
   PubMed Web of Science ®Google Scholar
• Shigeoka S, Onishi T, Nakano Y, et al. Characterization and physiological function of glutathione reductase in Euglena gracilis z. Biochem J. 1987;242:511–515.10.1042/bj2420511
   PubMed Web of Science ®Google Scholar
• Maruta T, Noshi M, Nakamura M, et al. Ferulic acid 5-hydroxylase 1 is essential for expression of anthocyanin biosynthesis-associated genes and anthocyanin accumulation under photooxidative stress in Arabidopsis. Plant Sci. 2014;219–220:61–68.10.1016/j.plantsci.2014.01.003
   PubMed Web of Science ®Google Scholar
• Gueta-Dahan Y, Yaniv Z, Zilinskas BA, et al. Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in Citrus. Planta. 1997;203:460–469.10.1007/s004250050215
   PubMed Web of Science ®Google Scholar
• Noshi M, Mori D, Tanabe N, et al. Arabidopsis clade IV TGA transcription factors, TGA10 and TGA9, are involved in ROS-mediated responses to bacterial PAMP flg22. Plant Sci. 2016;252:12–21.10.1016/j.plantsci.2016.06.019
   PubMed Web of Science ®Google Scholar
• Maruta T, Tanouchi A, Tamoi M, et al. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol. 2010;51:190–200.10.1093/pcp/pcp177
   PubMed Web of Science ®Google Scholar
• Dixon DP, Davis BG, Edwards R. 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. 2002;277:30859–30869.10.1074/jbc.M202919200
   PubMed Web of Science ®Google Scholar
• Foyer CH, Mullineaux PM. The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues. FEBS Lett. 1998;425:528–529.10.1016/S0014-5793(98)00281-6
   PubMed Web of Science ®Google Scholar
• Mhamdi A, Queval G, Chaouch S, et al. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot. 2010;61:4197–4220.10.1093/jxb/erq282
   PubMed Web of Science ®Google Scholar
• Noctor G, Queval G, Mhamdi A, et al. Glutathione. Arabidopsis Book. 2011;9:e0142.
   Google Scholar
• Noctor G, Mhamdi A, Chaouch S, et al. Glutathione in plants: an integrated overview. Plant Cell Environ. 2012;35:454–484.10.1111/j.1365-3040.2011.02400.x
   PubMed Web of Science ®Google Scholar
• Garcia-Gimenez JL, Markovic J, Dasi F, et al. Nuclear glutathione. Biochem Biophys Acta. 1830;2013:3304–3316.
   Google Scholar
• Queval G, Issakidis-Bourguet E, Hoeberichts FA, et al. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J. 2007;52:640–657.10.1111/j.1365-313X.2007.03263.x
   PubMed Web of Science ®Google Scholar
• Kwon SY, Choi SM, Ahn YO, et al. Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol. 2003;160:347–353.10.1078/0176-1617-00926
   PubMed Web of Science ®Google Scholar
• Le Martret B, Poage M, Shiel K, et al. Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J. 2011;9:661–673.10.1111/pbi.2011.9.issue-6
   PubMed Web of Science ®Google Scholar
• Vanderauwera S, Suzuki N, Miller G, et al. Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci USA. 2011;108:1711–1716.10.1073/pnas.1018359108
   PubMed Web of Science ®Google Scholar
• Johnston EJ, Rylott EL, Beynon E, et al. Monodehydroascorbate reductase mediates TNT toxicity in plants. Science. 2015;349:1072–1075.10.1126/science.aab3472
   PubMed Web of Science ®Google Scholar