Abstract
Ascorbate peroxidases (APXs) are, in general, photosynthetic eukaryote-specific enzymes, which catalyze the reduction of H2O2 using ascorbate as an electron donor. Considering the very low affinity of ascorbate with H2O2, the acquisition of APX was certainly an important event, allowing plants to use ascorbate for H2O2 metabolism. This also provides a plausible explanation for why plants accumulate a massive amount of ascorbate because this substrate is also required for stabilizing fragile APX enzymes (particularly chloroplastic isoforms). In higher plants, APXs are distributed in the cytosol, mitochondria, chloroplasts (both stroma and thylakoid membrane), and peroxisomes to modulate organellar and cellular levels of H2O2. Despite its potential toxicity, H2O2 is a relatively stable form of a reactive oxygen species, and consequently it can act as a key signaling molecule for plant stress responses. From this point of view, APXs also have a dual role, being antioxidant enzymes and H2O2 signaling regulators, and their balance is crucial for fine-tuning stress responses. In this chapter, we describe the physiological roles of APX isoforms in plants by overviewing the findings of biochemical, physiological, and genetic studies.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A (2007) A bacterial transgene for catalase protects translation of d1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol 145:258–265
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Aroca Á, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Awad J, Stotz HU, Fekete A, Krischke M, Engert C, Havaux M, Berger S, Mueller MJ (2015) 2-cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions. Plant Physiol 167:1592–1160
Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462
Bechtold U, Richard O, Zamboni A, Gapper C, Geisler M, Pogson B, Karpinski S, Mullineaux PM (2008) Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis. J Exp Bot 59:121–133
Bursey EH, Poulos TL (2000) Two substrate binding sites in ascorbate peroxidase: the role of arginine 172. Biochemistry 39:7374–7379
Chang CC, Slesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683
Chen GX, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998
Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877
Danna CH, Bartoli CG, Sacco F, Ingala LR, Santa-Maria GE, Guiamet JJ, Ugalde RA (2003) Thylakoid-bound ascorbate peroxidase mutant exhibits impaired electron transport and photosynthetic activity. Plant Physiol 132:2116–2125
Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281
de Pinto MC, Locato V, Sgobba A, Romero-Puertas Mdel C, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775
Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376–1387
Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM (2017) Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat Commun 8:49
Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Planta 119:355–364
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100
Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445
Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443
Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, Asami T, Davies WJ, Jones AM, Baker NR, Mullineaux PM (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–2162
Gelhaye E, Navrot N, Macdonald IK, Rouhier N, Raven EL, Jacquot JP (2006) Ascorbate peroxidase-thioredoxin interaction. Photosynth Res 89:193–200
Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53
Giacomelli L, Masi A, Ripoll DR, Lee MJ, van Wijk KJ (2007) Arabidopsis thaliana deficient in two chloroplast ascorbate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low. Plant Mol Biol 65:627–644
Gou JY, Li K, Wu K, Wang X, Lin H, Cantu D, Uauy C, Dobon-Alonso A, Midorikawa T, Inoue K, Sánchez J, Fu D, Blechl A, Wallington E, Fahima T, Meeta M, Epstein L, Dubcovsky J (2015) Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell 27:1755–1770
Granlund I, Storm P, Schubert M, Garcia-Cerdan JG, Funk C, Schroder WP (2009) The TL29 protein is lumenlocated, associated with PSII and not an ascorbate peroxidase. Plant Cell Physiol 50:1898–1910
Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154
Ishikawa T, Yoshimura K, Sakai K, Tamoi M, Takeda T, Shigeoka S (1998) Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol 39:23–34
Ishikawa T, Tajima N, Nishikawa H, Gao Y, Rapolu M, Shibata H, Sawa Y, Shigeoka S (2010) Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. Biochem J 426:125–134
Jiang L, Chen Z, Gao Q, Ci L, Cao S, Han Y, Wang W (2016) Loss-of-function mutations in the APX1 gene result in enhanced selenium tolerance in Arabidopsis thaliana. Plant Cell Environ 39:2133–2144
Jiang L, Wang W, Chen Z, Gao Q, Xu Q, Cao H (2017) A role for APX1 gene in lead tolerance in Arabidopsis thaliana. Plant Sci 256:94–102
Jung HS, Crisp PA, Estavillo GM, Cole B, Hong F, Mockler TC, Pogson BJ, Chory J (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proc Natl Acad Sci U S A 110:14474–14479
Kangasjärvi S, Lepistö A, Hännikäinen K, Piippo M, Luomala EM, Aro EM, Rintamäki E (2008) Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem J 412:275–285
Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640
Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657
Kieselbach T, Bystedt M, Hynds P, Robinson C, Schröder WP (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480:271–276
Kitajima S (2008) Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-cys peroxiredoxin. Photochem Photobiol 84:1404–1409
Kitajima S, Kitamura M, Koja N (2008) Triple mutation of Cys26, Trp35, and Cys126 in stromal ascorbate peroxidase confers H2O2 tolerance comparable to that of the cytosolic isoform. Biochem Biophys Res Commun 372:918–923
Kitajima S, Nii H, Kitamura M (2010) Recombinant stromal APX defective in the unique loop region showed improved tolerance to hydrogen peroxide. Biosci Biotechnol Biochem 74:1501–1503
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203
Lazzarotto F, Teixeira FK, Rosa SB, Dunand C, Fernandes CL, Fontenele Ade V, Silveira JA, Verli H, Margis R, Margis-Pinheiro M (2011) Ascorbate peroxidase-related (APx-R) is a new heme-containing protein functionally associated with ascorbate peroxidase but evolutionarily divergent. New Phytol 191:234–250
Lundberg E, Storm P, Schröder WP, Funk C (2011) Crystal structure of the TL29 protein from Arabidopsis thaliana: an APX homolog without peroxidase activity. J Struct Biol 176:24–31
Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51:190–200
Maruta T, Inoue T, Noshi M, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012a) Cytosolic ascorbate peroxidase 1 protects organelles against oxidative stress by wounding- and jasmonate-induced H2O2 in Arabidopsis plants. Biochim Biophys Acta 1820:1901–1907
Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012b) H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717–11729
Maruta T, Ojiri M, Noshi M, Tamoi M, Ishikawa T, Shigeoka S (2013) Activation of γ-aminobutyrate production by chloroplastic H2O2 is associated with the oxidative stress response. Biosci Biotechnol Biochem 77:422–425
Maruta T, Noshi M, Nakamura M, Matsuda S, Tamoi M, Ishikawa T, Shigeoka S (2014) Ferulic acid 5-hydroxylase 1 is essential for expression of anthocyanin biosynthesis-associated genes and anthocyanin accumulation under photooxidative stress in Arabidopsis. Plant Sci 219–220:61–68
Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386
Mhamdi A, Noctor G, Baker A (2012) Plant catalases: peroxisomal redox guardians. Arch Biochem Biophys 525:181–194
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19
Mittler R, Feng X, Cohen M (1998) Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10:461–473
Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, Inzé D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci U S A 96:14165–14170
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
Miyagawa Y, Tamoi M, Shigeoka S (2000) Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol 41:311–320
Miyake C, Asada K (1996) Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate; hydrogen peroxide decomposes compound I of ascorbate peroxidase. Plant Cell Physiol 37:423–430
Miyake C, Shinzaki Y, Nishioka M, Horiguchi S, Tomizawa K (2006) Photoinactivation of ascorbate peroxidase in isolated tobacco chloroplasts: Galdieria partita APX maintains the electron flux through the water-water cycle in transplastomic tobacco plants. Plant Cell Physiol 47:200–210
Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042
Nedelcu AM, Miles IH, Fagir AM, Karol K (2008) Adaptive eukaryote-to-eukaryote lateral gene transfer: stress-related genes of algal origin in the closest unicellular relatives of animals. J Evol Biol 21:1852–1860
Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594
Passardi F, Bakalovic N, Teixeira FK, Margis-Pinheiro M, Penel C, Dunand C (2007) Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes. Genomics 89:567–579
Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34:187–203
Queval G, Foyer CH (2012) Redox regulation of photosynthetic gene expression. Philos Trans R Soc Lond Ser B Biol Sci 367:3475–3485
Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakière B, Vanacker H, Miginiac-Maslow M, Van Breusegem F, Noctor G (2007) 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 52:640–657
Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M, Yang J, Schlögelhofer P, Mechtler K (2015) Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol Cell Proteomics 14:556–571
Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ 29:269–281
Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H (2010) ANKYRIN REPEAT-CONTAINING PROTEIN 2A is an essential molecular chaperone for peroxisomal membrane-bound ASCORBATE PEROXIDASE3 in Arabidopsis. Plant Cell 22:811–831
Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470
Shigeoka S, Nakano Y, Kitaoka S (1980) Metabolism of hydrogen peroxide in Euglena gracilis Z by L-ascorbic acid peroxidase. Biochem J 186:377–380
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30
Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa K, Yokota A, Shigeoka S (1998) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428:47–51
Szechyńska-Hebda M, Kruk J, Górecka M, Karpińska B, Karpiński S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22:2201–2218
Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J Mol Evol 59:761–770
Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314
Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J (2014) Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21:1422–1441
Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45–58
Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S, Ravanat JL, Hegie A, Triantaphylidès C, Shulaev V, Van Montagu MC, Van Breusegem F, Mittler R (2011) Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci U S A 108:1711–1716
Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732
Welinder KG (1992) Superfamily of plant, fungal and bacterial peroxidases. Curr Opin Struct Biol 2:388–393
Willems P, Mhamdi A, Stael S, Storme V, Kerchev P, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS wheel: refining ROS transcriptional footprints. Plant Physiol 171:1720–1733
Xu L, Carrie C, Law SR, Murcha MW, Whelan J (2013) Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol 161:644–662
Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid-membrane bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32:915–926
Yabuta Y, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol 45:1586–1594
Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162
Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615
Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol 123:223–234
Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2002) Identification of a cis element for tissue-specific alternative splicing of chloroplast ascorbate peroxidase pre-mRNA in higher plants. J Biol Chem 277:40623–40632
Zámocký M, Gasselhuber B, Furtmüller PG, Obinger C (2014) Turning points in the evolution of peroxidase-catalase superfamily: molecular phylogeny of hybrid heme peroxidases. Cell Mol Life Sci 71:4681–4696
Acknowledgement
This work was partially supported by the Ministry of Education, Culture, Sports, Science, and Technology of Japan [Grant-in-Aid for Scientific Research (B) (to T.I and T.M: 17H03807)].
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Maruta, T., Ishikawa, T. (2017). Ascorbate Peroxidases: Crucial Roles of Antioxidant Enzymes in Plant Stress Responses. In: Hossain, M., Munné-Bosch, S., Burritt, D., Diaz-Vivancos, P., Fujita, M., Lorence, A. (eds) Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-74057-7_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-74057-7_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-74056-0
Online ISBN: 978-3-319-74057-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)