Skip to main content
SpringerLink
Log in

Ascorbate Peroxidases: Scavengers or Sensors of Hydrogen Peroxide Signaling?

  • Chapter
  • First Online:
Redox Homeostasis in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Environmental factors can trigger the accumulation of reactive oxygen species (ROS) in plant cells. These molecules at a basal level are associated with essential cellular functions such as signaling for both developmental and defense responses in plants. On the other hand, ROS at high concentrations are significantly detrimental, leading to oxidative damage in different cell biomolecules. Plants have efficient antioxidant systems to neutralize toxic levels of ROS, which include various enzymatic and non-enzymatic components. Ascorbate peroxidase (APX) is a key enzyme in this context, acting in the control of toxic ROS levels in different subcellular compartments. In several species, APX expression is modulated in some developmental stages, and under biotic and abiotic stresses, indicating the importance of APX activity in controlling hydrogen peroxide (H2O2) content in intracellular compartments. The genetic manipulation of APX gene expression in diverse plant models has been found to trigger differential responses to stress conditions and affects the growth and development of the plant, indicating that these enzymes can play a role as H2O2 scavengers and also as sensors of redox alteration inside plant cells.

Andréia Caverzan, Douglas Jardim-Messeder and Ana Luiza Paiva—These authors contributed equally.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal GK, Jwa NS, Iwahashi H, Rakwal R (2003) Importance of ascorbate peroxidases OsAPX1 and OsAPX2 in the rice pathogen response pathways and growth and reproduction revealed by their transcriptional profiling. Gene 11:93–103

    Article  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DL, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier Scientific Publishers, Amsterdam, pp 227–287

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121:231–238

    Article  CAS  PubMed  Google Scholar 

  • Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS ONE 6:e20714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker A, Graham I (2002) Plant peroxisomes. Biochemistry, cell biology and biotechnological applications. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64:1121–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begara-Morales JC, Sanchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilha MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  CAS  PubMed  Google Scholar 

  • Bonifacio A, Martins MO, Ribeiro CW, Fontenele AV, Carvalho FE, Margis-Pinheiro M, Silveira JA (2011) Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant, Cell Environ 34:1705–1722

    Article  CAS  Google Scholar 

  • Bonifacio A, Carvalho FEL, Martins MO, Lima Neto MC, Cunha JR, Ribeiro CW, Margis-Pinheiro M, Silveira JAG (2016) Silenced rice in both cytosolic ascorbate peroxidases displays pre-acclimation to cope with oxidative stress induced by 3-aminotriazole-inhibited catalase. J Plant Physiol 201:17–27

    Article  CAS  PubMed  Google Scholar 

  • Battistuzzi G, D’Onofrio M, Loschi L, Sola M (2001) Isolation and characterization of two peroxidases from Cucumis sativus. Arch Biochem Biophys 388:100–112

    Article  CAS  PubMed  Google Scholar 

  • Boveris AH, Sies H, Martino EE, Decampo R, Turreus JF, Stoppani AOM (1980) Deficient metabolic utilization of hydrogen peroxide in Trypanosoma cruzi. Biochem J 188:643–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inzé D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase, a prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camillo LR, Filadelfo CR, Monzani PS, Corrêa RX, Gramacho KP, Micheli F, Pirovani CP (2013) Tc-cAPX, a cytosolic ascorbate peroxidase of Theobroma cacao L. engaged in the interaction with Moniliophthora perniciosa, the causing agent of witches’ broom disease. Plant Physiol Biochem 73:254–265

    Article  CAS  PubMed  Google Scholar 

  • Cao S, Du XH, Li LH, Liu YD, Zhang L, Pan X, Li Y, Li H, Lu H (2017) Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants. Russ J Plant Physiol 64:224–234

    Article  CAS  Google Scholar 

  • Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caverzan A, Bonifacio A, Carvalho FEL, Andrade CMB, Passaia G, Schünemann M, Maraschin FS, Martins MO, Teixeira FK, Rauber R, Margis R, Silveira JAG, Margis-Pinheiro M (2014) The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice. Plant Sci 214:74–87

    Article  CAS  PubMed  Google Scholar 

  • Caverzan A, Casassola A, Brammer AP (2016) Reactive oxygen species and antioxidant enzymes. In: Shanker AK, Shanker C (eds) Abiotic and biotic stress in plants—recent advances and future perspectives involved in plant tolerance to stress. Intech, Croatia, pp 463–480

    Google Scholar 

  • Chen GX, Asada K (1989) APX in tea leaves, occurrence of two isoenzymes, the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    Article  CAS  Google Scholar 

  • Chen Y, Wang H, Wang X, Cao A, Chen P (2006) Cloning and expression of peroxisomal ascorbate peroxidase gene from wheat. Mol Biol Rep 33:207–213

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Letnik I, Hacham Y, Dobrev P, Ben-Daniel BH, Vanková R, Amir R, Miller G (2014) Ascorbate peroxidase 6 protects Arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, abscisic acid, and auxin. Plant Physiol 166:370–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Cai J, Yang FX, Zhou B, Zhou LR (2015) Ascorbate peroxidase from Jatropha curcas enhances salt tolerance in transgenic Arabidopsis. Genet Mol Res 14:4879–4889

    Article  CAS  PubMed  Google Scholar 

  • Chew O, Whelan J, Millar H (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

    Article  PubMed  Google Scholar 

  • Chiang CM, Chen LFO, Shih SW, Lin KH (2015a) Expression of eggplant ascorbate peroxidase increases the tolerance of transgenic rice plants to flooding stress. J Plant Biochem Biotechnol 24:257–267

    Article  CAS  Google Scholar 

  • Chiang CM, Chien HL, Chen LFO, Hsiung TC, Chiang MC, Chen SP, Lin KH (2015b) Overexpression of the genes coding ascorbate peroxidase from Brassica campestris enhances heat tolerance in transgenic Arabidopsis thaliana. Biol Plantarum 59:305–315

    Article  CAS  Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • Collen J, Rıo MJD, Garcıa-Reina G, Pedersen M (1995) Photosynthetic production of hydrogen peroxide by Ulva rigida C. Ag. (Chlorophyta). Planta 196:225–230

    Article  CAS  Google Scholar 

  • Corpas FJ (2015) What is the role of hydrogen peroxide in plant peroxisomes? Plant Biol (Stuttg) 17:1099–1103

    Article  CAS  Google Scholar 

  • Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013) Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot 64:3339–3349

    Article  CAS  PubMed  Google Scholar 

  • Cunha JR, Lima Neto MC, Carvalho FEL, Martins MO, Jardim-Messeder D, Margis-Pinheiro M, Silveira JAG (2016) Salinity and osmotic stress trigger different antioxidant responses related to cytosolic ascorbate peroxidase knockdown in rice roots. Environ Exp Bot 131:58–67

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Article  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • Davletova S, Rizhsky L, Liang HJ, Zhong SQ, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Leonardis S, Dipierro N, Dipierro S (2000) Purification and characterization of an APX from potato tuber mitochondria. Plant Physiol Biochem 38:773–779

    Article  Google Scholar 

  • De Pinto MC, Locato V, Sgobba A, Romero-Puertas MC, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272

    Article  PubMed  Google Scholar 

  • Dong C, Zheng XF, Li GL, Pan C, Zhou MQ, Hu ZL (2011) Cloning and expression of one chloroplastic ascorbate peroxidase gene from Nelumbo nucifera. Biochem Genet 49:656–664

    Article  CAS  PubMed  Google Scholar 

  • Duan M, Feng HL, Wang LY, Li D, Meng QW (2012) Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol 169:867–877

    Article  CAS  PubMed  Google Scholar 

  • Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–2613

    Article  CAS  PubMed  Google Scholar 

  • Faize M, Burgos L, Faize L, Petri C, Barba-Espin G, Díaz-Vivancos P, Clemente-Moreno MJ, Alburquerque N, Hernandez JA (2012) Modulation of tobacco bacterial disease resistance using cytosolic ascorbate peroxidase and Cu, Zn-superoxide dismutase. Plant Pathol 61:858–866

    Article  CAS  Google Scholar 

  • Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J 33:691–705

    Article  CAS  PubMed  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Breusegem FV (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35

    Article  CAS  PubMed  Google Scholar 

  • Gelhaye E, Navrot N, Macdonald IK, Rouhier N, Raven EL, Jacquot JP (2006) Ascorbate peroxidase-thioredoxin interaction. Photosynth Res 89:193–200

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan Q, Xia D, Liu S (2010) OsAPX4 gene response to several environmental stresses in rice (Oryza sativa L.). Afr J Biotechnol 9:5908–5913

    CAS  Google Scholar 

  • Guan Q, Wang Z, Wang X, Takano T, Liu S (2015) A peroxisomal APX from Puccinellia tenuiflora improves the abiotic stress tolerance of transgenic Arabidopsis thaliana through decreasing of H2O2 accumulation. J Plant Physiol 175:183–191

    Article  CAS  PubMed  Google Scholar 

  • Groden D, Beck E (1979) H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim Biophys Acta 546:426–435

    Article  CAS  PubMed  Google Scholar 

  • Hernández JA, Jiménez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant, Cell Environ 23:853–862

    Article  Google Scholar 

  • Hirooka S, Misumi O, Yoshida M, Mori T, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Kuroiwa H, Kuroiwa T (2009) Expression of the Cyanidioschyzon merolae stromal ascorbate peroxidase in Arabidopsis thaliana enhances thermotolerance. Plant Cell Rep 28:1881–1893

    Article  CAS  PubMed  Google Scholar 

  • Huang AHC, Trelease RN, Moore TS (1983) Plant peroxisomes. Academic Press, New York

    Google Scholar 

  • Ishikawa T, Sakai K, Yoshimura K, Takeda T, Shigeoka S (1996) cDNAs encoding spinach stromal thylakoid bound ascorbate peroxidase, differing in the presence or absence of their 39-coding regions. FEBS Lett 384:289–293

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Yoshimura K, Tamoi M, Takeda T, Shigeoka S (1997) Alternative mRNA splicing of 39-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplast. Biochem J 328:795–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M, Galina A (2015) Succinate dehydrogenase (mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. New Phytol 208:776–789

    Article  CAS  PubMed  Google Scholar 

  • Jespersen HM, KjaersgardIvh OL, Welinder KG (1997) From sequence analysis of three novel APXs from Arabidopsis thaliana to structure, function and evolution of seven types of APX. Biochem J 326:305–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang G, Yin D, Zhao J, Chen H, Guo L, Zhu L, Zhai W (2016a) The rice thylakoid membrane-bound ascorbate peroxidase OsAPX8 functions in tolerance to bacterial blight. Sci Rep 6:26104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang M, Jiang JJ, He CM, Guan M (2016b) Broccoli plants over-expressing a cytosolic ascorbate peroxidase gene increase resistance to downy mildew and heat stress. J Plant Pathol 98:413–420

    Google Scholar 

  • Jimenez A, Hernandez JA, Del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kapoor D, Sharma R, Handa N, Kaur H, Rattan A, Yadav P, Gautam V, Kaur R, Bhardwaj R (2015) Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:13

    Article  Google Scholar 

  • Karyotou K, Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Arch Biochem Biophys 434:248–257

    Article  CAS  PubMed  Google Scholar 

  • Kavitha K, Venkatamaranm G, Parida A (2008) An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization. Plant Physiol Biochem 46:794–804

    Article  CAS  PubMed  Google Scholar 

  • Kelly GJ, Latzko E (1979) Soluble ascorbate peroxidase, detection in plants and use in vitamin C estimation. Naturwissenschaften 66:617–619

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuźniak E, Skłodowska M (1999) The effect of Botrytis cinerea infection on ascorbate–glutathione cycle in tomato leaves. Plant Sci 148:69–76

    Article  Google Scholar 

  • Kuźniak E, Skłodowska M (2001) Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Sci 160:723–731

    Article  PubMed  Google Scholar 

  • Kuźniak E, Skłodowska M (2004) The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves. J Exp Bot 55:605–612

    Article  PubMed  Google Scholar 

  • Lázaro JL, Jiménez A, Camejo D, Iglesias-Baena I, Martí MC, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460

    Google Scholar 

  • Lazzarotto F, Turchetto-Zolet AC, Margis-Pinheiro M (2015) Revisiting the non-animal peroxidase superfamily. Trends Plant Sci 20:1–7

    Article  CAS  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Li YJ, Hai RL, Du XH, Jiang XN, Lu H (2009) Over-expression of a Populus peroxisomal ascorbate peroxidase (PpAPX) gene in tobacco plants enhances stress tolerance. Plant Breed 128:404–410

    Article  CAS  Google Scholar 

  • Li Z, Su D, Lei B, Wang F, Geng W, Pan G, Cheng F (2015) Transcriptional profile of genes involved in ascorbate–glutathione cycle in senescing leaves for an early senescence leaf (esl) rice mutant. J Plant Physiol 176:1–15

    Article  CAS  PubMed  Google Scholar 

  • Lisenbee CS, Heinze M, Trelease RN (2003) Peroxisomal APX resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells. Plant Physiol 132:870–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu KL, Shen L, Wang JQ, Sheng JP (2008) Rapid inactivation of chloroplastic ascorbate peroxidase is responsible for oxidative modification to Rubisco in tomato (Lycopersicon esculentum) under cadmium stress. J Integr Plant Biol 50:415–426

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Bao H, Cai J, Han J, Zhou L (2014) A novel thylakoid ascorbate peroxidase from Jatropha curcas enhances salt tolerance in transgenic tobacco. Int J Mol Sci 15:171–185

    Article  CAS  Google Scholar 

  • Locato V, de Pinto MC, De Gara L (2009) Different involvement of the mitochondrial, plastidial and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Physiol Plant 135:296–306

    Article  CAS  PubMed  Google Scholar 

  • López-Huertas E, Corpas FJ, Sandalio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Huertas E, del Río LA (2014) Characterization of antioxidant enzymes and peroxisomes of olive (Olea europaea L.) fruits. J Plant Physiol 171:1463–1471

    Article  CAS  PubMed  Google Scholar 

  • Lozano-Juste J, Colom-Moreno R, Leon J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Z, Liu D, Liu S (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917

    Article  CAS  PubMed  Google Scholar 

  • Luo Q, Peng M, Zhang X, Lei P, Ji X, Chow W, Meng F, Sun G (2017) Comparative mitochondrial proteomic, physiological, biochemical and ultrastructural profiling reveal factors underpinning salt tolerance in tetraploid black locust (Robinia pseudoacacia L.). BMC Genomics 18:648

    Google Scholar 

  • Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY–2 cells. Physiol Plant 117:550–557

    Article  CAS  PubMed  Google Scholar 

  • Mandelman D, Jamal J, Poulos TL (1998a) Identification of two electron-transfer sites in ascorbate peroxidase using chemical modification, enzyme kinetics crystallography. Biochemistry 37:17610–17617

    Article  CAS  PubMed  Google Scholar 

  • Mandelman D, Schwarz FP, Li H, Poulos TL (1998b) The role of quaternary interactions on the stability activity of ascorbate peroxidase. Protein Sci 7:2089–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mano S, Yamaguchi K, Hayashi M, Nishimura M (1997) Stromal thylakoid-bound ascorbate peroxidases are produced by alternative splicing in pumpkin. FEBS Lett 413:21–26

    Article  CAS  PubMed  Google Scholar 

  • Mano J, Ohno C, Domae Y, Asada K (2001) Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochim Biophys Acta 1504:275–287

    Article  CAS  PubMed  Google Scholar 

  • Marchand C, Le MP, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4:2696–2706

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012) H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717–11729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menezes-Benavente L, Teixeira FK, Kamei CLA, Margis-Pinheiro M (2004) Salt stress induces altered expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.) Plant Sci 166:323–331

    Google Scholar 

  • Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–17785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Zilinskas BA (1991) Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol 97:962–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem VF (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2017) ROS are good? Trends Plant Sci 22:11–19

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant, Cell Environ 26:845–856

    Article  CAS  Google Scholar 

  • Mittova V, Guy M, Tal M, Volokita M (2004a) Salinity upregulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Theodoulou FL, Kiddle G, Volokita M, Tal M, Foyer CH, Guy M (2004b) Comparison of mitochondrial APX in the cultivated tomato, Lycopersicon esculentum, its wild, salt-tolerant relative, L. pennellii—role for matrix isoforms in protection against oxidative damage. Plant, Cell Environ 27:237–250

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Michihata F, Asada K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol 32:33–43

    CAS  Google Scholar 

  • Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553

    CAS  Google Scholar 

  • Miyake C, Cao WH, Asada K (1993) Purification and molecular properties of thylakoid-bound ascorbate peroxidase from spinach chloroplasts. Plant Cell Physiol 343:881–889

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  Google Scholar 

  • Morita S, Nakatani S, Koshiba T, Masumura T, Ogihara Y, Tanaka K (2011) Differential expression of two cytosolic ascorbate peroxidases and two superoxide dismutase genes in response to abiotic stress in rice. Rice Sci 18:157–166

    Article  Google Scholar 

  • Mullen RT, Trelease RN (2000) The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J Biol Chem 275:16337–16344

    Article  CAS  PubMed  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 8:940–953

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione—keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Nulton-Persson AC, Szweda LI (2001) Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem 276:23357–23361

    Article  CAS  PubMed  Google Scholar 

  • Ogawa K, Kanematsu S, Takabe K, Asada K (1995) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immunogold labeling after rapid freezing and substitution method. Plant Cell Physiol 36:565–573

    CAS  Google Scholar 

  • Orvar L, Ellis BE (1997) Transgenic tobacco expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J 11:1297–1305

    Article  CAS  Google Scholar 

  • Panchuk I, Volkov R, Schöffl F (2002) Heat stress and heat shock transcription factor-dependent expression and activity of APX in Arabidopsis. Plant Physiol 129:838–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panchuk II, Zentgraf U, Volkov RA (2005) Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana. Planta 222:926–932

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:581

    Article  PubMed  PubMed Central  Google Scholar 

  • Passaia G, Margis-Pinheiro M (2015) Glutathione peroxidases as redox sensor proteins in plant cells. Plant Sci 234:22–26

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140

    Article  CAS  PubMed  Google Scholar 

  • Pereira CS, Da Costa DS, Teixeira J, Pereira S (2005) Organ-specific distribution and subcellular localization of APX isoenzymes in potato Solanum tuberosum L. plants. Protoplasma 226:223–230

    Article  CAS  PubMed  Google Scholar 

  • Pitcher LH, Repetti P, Zilinskas BA (1994) Overexpression of ascorbate peroxidase protects plants from oxidative stress. Plant physiol (suppl.) 105:116

    Google Scholar 

  • 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 34:185–201

    Article  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro CW, Carvalho FEL, Rosa SB, Alves-Ferreira M, Andrade CMB, Ribeiro-Alves M, Silveira JAG, Margis R, Margis-Pinheiro M (2012) Modulation of genes related to specific metabolic pathways in response to cytosolic ascorbate peroxidase knockdown in rice plants. Plant Biol 14:944–955

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro CW, Korbes AP, Garighan JA, Jardim-Messeder D, Carvalho FEL, Sousa RHV, Caverzan A, Teixeira FK, Silveira JAG, Margis-Pinheiro M (2017) Rice peroxisomal ascorbate peroxidase knockdown affects ROS signaling and triggers early leaf ssenescence. Plant Sci 263:55–65

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gómez M, del Río LA (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:S25–S31

    Article  CAS  PubMed  Google Scholar 

  • Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JA, Ferreira-Silva SL, Abreu-Neto J, Margis R, Margis-Pinheiro M (2010) Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71:548–558

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long-term salt stress. Plant Sci 162:897–904

    Article  CAS  Google Scholar 

  • Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, Tanida M (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52:45–151

    Article  Google Scholar 

  • Sato Y, Masuta Y, Saito K, Murayama S, Ozawa K (2011) Enhanced chilling tolerance at the booting stage in rice by transgenic overexpression of the ascorbate peroxidase gene OsAPXa. Plant Cell Rep 30:399–406

    Article  CAS  PubMed  Google Scholar 

  • Saxena SC, Joshi P, Grimm B, Arora S (2011) Alleviation of ultraviolet-C induced oxidative through overexpression of cytosolic ascorbate peroxidase. Biologia 66:1052–1059

    Article  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian J Medic Biologic Res 38:995–1014

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2004) APX from rice seedlings, properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Botany 2012:1–26

    Article  CAS  Google Scholar 

  • Shi WM, Muramoto Y, Ueda A, Takabe T (2001) Cloning of peroxisomal ascorbate peroxidase gene from barley and enhanced thermotolerance by overexpressing in Arabidopsis thaliana. Gene 273:23–27

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T, Takeda T, Yamauchi Y, 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

    Article  CAS  PubMed  Google Scholar 

  • Shrivastava DC, Kisku AV, Saxena M, Deswal R, Sarin NB (2015) Stress inducible cytosolic ascorbate peroxidase (Ahcapx) from Arachis hypogaea cell lines confers salinity and drought stress tolerance in transgenic tobacco. The Nucleus 58:3–13

    Article  Google Scholar 

  • Singh N, Mishra A, Jha B (2014) Over-expression of the Peroxisomal Ascorbate Peroxidase (SbpAPX) Gene Cloned from halophyte Salicornia brachiata confers salt and drought stress tolerance in transgenic tobacco. Mar Biotechnol 16:321–332

    Article  CAS  Google Scholar 

  • Song XS, Wang YJ, Mao WH, Shi K, Zhou YH, Nogués S, Yu JQ (2009) Effects of cucumber mosaic virus infection on electron transport and antioxidant system in chloroplasts and mitochondria of cucumber and tomato leaves. Physiol Plant 135:246–257

    Article  CAS  PubMed  Google Scholar 

  • Sukweenadhi J, Kim YJ, Rahimi S, Silva J, Myagmarjav D, Kwon WS, Yang DC (2017) Overexpression of a cytosolic ascorbate peroxidase from Panax ginseng enhanced salt tolerance in Arabidopsis thaliana. Plant Cell Tiss Organ Cult 129:337–350

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2013) Fisiologia vegetal. Artmed, Porto Alegre

    Google Scholar 

  • Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. The Plant J 72:585–599

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tretter L, Adam-Vizi V (2000) Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 20:8972–8979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaahtera L, Brosche M, Wrzaczek M, Kangasjarvi J (2014) Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21:1422–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 276:643–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vighi IL, Benitez LC, Amaral MN, Moraes GP, Auler PA, Rodrigues GS, Deuner S, Maia LC, Braga EJB (2017) Functional characterization of the antioxidant enzymes in rice plants exposed to salinity stress. Biol Plantarum 61:540–550

    Article  CAS  Google Scholar 

  • Wada N, Kinoshita S, Matsuo M, Amako K, Miyake C, Asada K (1998) Purification and molecular properties of ascorbate peroxidase from bovine eye. Biochem Biophys Res Commun 242:256–261

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wisniewski M, Meilan R, Cui M, Webb R, Fuchigami L (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. JASHS 130:167–173

    CAS  Google Scholar 

  • Wang Y, Wu J, Choi YW, Jun TH, Kwon SW, Choi IS, Kim YC, Gupta R, Kim ST (2015) Expression analysis of Oryza sativa ascorbate peroxidase 1 (OsAPx1) in response to different phytohormones and pathogens. J Life Sci 25:1091–1097

    Article  Google Scholar 

  • Wang L, Zhao R, Zheng Y, Chen L, Li R, Ma J, Hong X, Ma P, Sheng J, Shen L (2017) SlMAPK1/2/3 and Antioxidant enzymes are associated with H2O2-induced chilling tolerance in tomato plants. J Agri Food Chem 65:6812–6820

    Article  CAS  Google Scholar 

  • Webb RP, Allen RD (1996) Overexpression of pea cytosolic ascorbate peroxidase confers protection against oxidative stress in transgenic Nicotiana tabacum. Plant Physiol 99:912–918

    Article  Google Scholar 

  • Welinder KG (1992) Superfamily of plant, fungal and bacterial peroxidases. Curr Opin Struct Biol 2:388–393

    Article  CAS  Google Scholar 

  • Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–653

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Wang G, Ji J, Gao H, Guan W, Wu J, Guan C, Wang Y (2014) Cloning of a cytosolic ascorbate peroxidase gene from Lycium chinense Mill. and enhanced salt tolerance by overexpressing in tobacco. Gene 543:85–92

    Article  CAS  PubMed  Google Scholar 

  • Xu WF, Shi WM, Liu F, Ueda A, Takabe T (2008) Enhanced zinc and cadmium tolerance and accumulation in transgenic Arabidopsis plants constitutively overexpressing a barley gene (HvAPX1) that encodes a peroxisomal ascorbate peroxidase. Botany 86:567–575

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 32:915–925

    Article  CAS  PubMed  Google Scholar 

  • Yadav P, Yadav T, Kumar S, Rani B, Kumar S, Jain V, Malhotra SP (2014) Partial purification and characterization of ascorbate peroxidase from ripening ber (Ziziphus mauritiana L.) fruits. Afr J Biotechnol 13:3323–3331

    Article  CAS  Google Scholar 

  • Yamaguchi K, Mori H, Nishimura M (1995a) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takeuchi Y, Mori H, Nishimura M (1995b) Development of microbody membrane proteins during the transformation of glyoxysomes to leaf peroxisomes in pumpkin cotyledons. Plant Cell Physiol 36:455–464

    Article  CAS  Google Scholar 

  • Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T (2004) Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol 45:18–27

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Wang J, Tissue D, Holaday AS, Allen R, Zhang H (2003) Photosynthesis and seed production under water-deficit conditions in transgenic tobacco plants that overexpress an Arabidopsis ascorbate peroxidase gene. Crop Sci 43:1477–1483

    Article  CAS  Google Scholar 

  • Yoshimura K, Ishikawa T, Nakamura Y, TamoiM Takeda T, Tada T, Nishimura K, Shigeoka S (1998) Comparative study on recombinant chloroplastic and cytosolic ascorbate peroxidase isozymes of spinach. Arch Biochem Biophys 353:55–63

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol 123:223–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaharieva T, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione related enzymes in sugar beet roots. Protoplasma 221:269–275

    CAS  PubMed  Google Scholar 

  • Zamocky 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wang J, Nickel U, Allen RD, Goodman HM (1997) Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase. Plant Mol Biol 34:967–971

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qiu Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS ONE 8:e57472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Ma C, Xue X, Xu M, Li J, Wu JX (2014) Overexpression of a cytosolic ascorbate peroxidase gene, OsAPX2, increases salt tolerance in transgenic alfalfa. J Integr Agric 13:2500–2507

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculdade de Agronomia e Medicina Veterinária, Programa de Pós-Graduação em Agronomia, Universidade de Passo Fundo, Passo Fundo, RS, 99052-900, Brazil

    Andréia Caverzan

  2. Departamento de Genética, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil

    Douglas Jardim-Messeder

  3. Departamento de Genética, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9500, Porto Alegre, RS, 91501-970, Brazil

    Ana Luiza Paiva & Marcia Margis-Pinheiro

Authors
  1. Andréia Caverzan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas Jardim-Messeder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Luiza Paiva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcia Margis-Pinheiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcia Margis-Pinheiro .

Editor information

Editors and Affiliations

  1. Department of Life Science and Bioinformatics, Assam University, Silchar, India

    Sanjib Kumar Panda

  2. Plant Molecular Physiology Lab, Gifu University, Gifu, Japan

    Yoshiharu Y. Yamamoto

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Caverzan, A., Jardim-Messeder, D., Paiva, A.L., Margis-Pinheiro, M. (2019). Ascorbate Peroxidases: Scavengers or Sensors of Hydrogen Peroxide Signaling?. In: Panda, S., Yamamoto, Y. (eds) Redox Homeostasis in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-95315-1_5

Download citation

Publish with us

Policies and ethics

Search

Navigation