Skip to main content
Log in

Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Extracellularly secreted plant peroxidases (POXs) are considered to catalyze the generation of reactive oxygen species (ROS) coupled to oxidation of plant hormone indole-3-acetic acid (IAA) and defense-related compounds salicylic acid (SA), aromatic monoamines (AMAs) and chitooligosaccharides (COSs). This review article consists of two parts, which describe H2O2-dependent and H2O2-independent mechanisms for ROS generation, respectively. Recent studies have shown that plant POXs oxidize SA, AMAs and COSs in the presence of H2O2 via a conventional POX cycle, yielding the corresponding radical species, such as SA free radicals. These radical species may react with oxygen, and superoxide (O2 ·−) is produced. Through the series of reactions 2 moles of O2 ·− can be formed from 1 moles of H2O2, thus leading to oxidative burst. It has been revealed that the ROS induced by SA, AMAs and COSs triggers the increase in cytosolic Ca2+ concentration. Actually POXs transduce the extracellular signals into the redox signals that eventually stimulate the intracellular Ca2+ signaling required for induction of defense responses. On the other hand, IAA can react with oxygen and plant POXs in the absence of H2O2, by forming the ternary complex enzyme-IAA-O2, which readily dissociates into enzyme, IAA radicals and O2 ·−. This article covers the recent reports showing that extracellularly produced hydroxy radicals derived from O2 ·− mediate the IAA-induced cell elongation. Here a novel model for IAA signaling pathway mediated by extracellular ROS produced by cell-wall POXs is proposed. In addition, possible controls of the IAA-POX reactions by a fungal alkaloid are discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2A, B.
Fig. 3A–D.
Fig. 4.

Similar content being viewed by others

References

  • Alayash AI (1999) Hemoglobin-based blood substitutes: oxygen carriers, pressor agents, or oxidants? Nat Biotechnol 17:545–549

    Article  CAS  PubMed  Google Scholar 

  • Beguiristain T, Lapeyrie F (1997) Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytol 136:525–532

    Article  CAS  Google Scholar 

  • Beguiristain T, Cote R, Rubini P, Jay-Allemand C, Lapeyrie F (1995) Hypaphorine accumulation in hyphae of the ectomycorrhizal fungus Pisolithus tinctorius. Phytochemistry 40:1089–1091

    Article  Google Scholar 

  • Bolwell GP (1995) The origin of the oxidative burst in plants. Free Rad Res 23:517–532

    CAS  Google Scholar 

  • Cervantes E (2001) ROS in root gravitropism: the auxin messengers? Trends Plant Sci 6:556–556

    Article  CAS  Google Scholar 

  • Chen SX, Schopfer P (1999) Hydroxyl-radical production in physiological reactions. A novel function of peroxidase. Eur J Biochem 260:726–735

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance induced by salicylic acid. Science 262:1883–1886

    CAS  PubMed  Google Scholar 

  • Ditengou FA, Lapeyrie F (2000) Hypaphorine from the ectomycorrhizal fungus Pisolithus tinctorius counteracts activities of indole-3-acetic acid and ethylene but not synthetic auxins in eucalypt seedlings. Mol Plant Microbe Interact 13:151–158

    CAS  PubMed  Google Scholar 

  • Ditengou FA, Beguiristain T, Lapeyrie F (2000) Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorrhizal fungus Pisolithus tinctorius, and restored by indole-3-acetic acid. Planta 211:722–728

    Article  CAS  PubMed  Google Scholar 

  • Frahry G, Schopfer P (2001) NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:175–183.

    CAS  PubMed  Google Scholar 

  • Gazarian IG, Lagrimini LM (1998) Anaerobic stopped-flow studies of indole-3-acetic acid oxidation by dioxygen catalyzed by horseradish peroxidase C and anionic tobacco peroxidase at neutral pH:catalase effect. Biophys Chem 72:231–237

    Article  CAS  Google Scholar 

  • Gazarian IG, Lagrimini LM, Mellon FA, Naldrett MJ, Ashby GA, Thorneley RNF (1998) Identification of skatolyl hydroperoxide and its role in the peroxidase-catalyzed oxidation of indol-3-yl acetic acid. Biochem J 333:223–232

    CAS  PubMed  Google Scholar 

  • Gazaryan IG, Lagrimini LM (1996a) Tobacco anionic peroxidase overexpressed in transgenic plants: Aerobic oxidation of indole-3-acetic acid. Phytochemistry 42:1271–1278

    Article  CAS  Google Scholar 

  • Gazaryan IG, Lagrimini LM (1996b) Purification and unusual kinetic properties of a tobacco anionic peroxidase. Phytochemistry 41:1029–1034

    Article  CAS  PubMed  Google Scholar 

  • Gazaryan IG, Lagrimini LM, Ashby GA, Thorneley NF (1996) Mechanism of indole-3-acetic acid oxidation by plant peroxidases: anaerobic stopped-flow spectrophotometric studies on horseradish and tobacco peroxidases. Biochem J 313:841–847

    CAS  PubMed  Google Scholar 

  • Goodwin DC, Grover TA, Aust ST (1997) Roles of efficient substrates in enhancement of peroxidase-catalyzed oxidations. Biochemistry 36:139–147

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Esttelle M (2000) Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem Sci 25:133–138

    PubMed  Google Scholar 

  • Hilaire E, Paulsen AQ, Brown CS, Guikema JA (1995) Microgravity and clinorotation cause redistribution of free calcium in sweet clover Columella cells. Plant Cell Physiol 36:831–837

    CAS  PubMed  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468

    Article  CAS  PubMed  Google Scholar 

  • Jiang MY, Zhang JH (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Google Scholar 

  • Jiang M, Zhang J (2002) Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215:1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Jones AM, Prasad PV (1992) Auxin-binding proteins and their possible roles in auxin-mediated plant cell growth. BioEssays 14:43–48

    CAS  Google Scholar 

  • Jones AM, Im KH, Savka MA, Wu MJ, DeWitt NG, Shillito R, Binns AN (1998) Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282:1114–1117

    CAS  PubMed  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060

    Article  CAS  PubMed  Google Scholar 

  • Kagan VE, Serbinova EA, Packer L (1990) Generation and recycling of radicals from phenolic antioxidants. Arch Biochem Biophys 280:33–39

    CAS  PubMed  Google Scholar 

  • Kawano T, Muto S (2000) Mechanism of peroxidase actions for salicylic acid-induced generation of active oxygen species and an increase in cytosolic calcium in tobacco suspension culture. J Exp Bot 51:685–693

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S (1998) Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: The earliest events in salicylic acid signal transduction. Plant Cell Physiol 39:721–730

    CAS  Google Scholar 

  • Kawano T, Pinontoan R, Uozumi N, Miyake C, Asada K, Kolattukudy PE, Muto S (2000a) Aromatic monoamine-induced immediate oxidative burst leading to an increase in cytosolic Ca2+ concentration in tobacco suspension culture. Plant Cell Physiol 41:1251–1258

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Pinontoan R, Uozumi N, Morimitsu Y, Miyake C, Asada K, Muto S (2000b) Phenylethylamine-induced generation of reactive oxygen species and ascorbate free radicals in tobacco suspension culture: mechanism for oxidative burst mediating Ca2+ influx. Plant Cell Physiol 41:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Sahashi N, Uozumi N, Muto S (2000c) Involvement of apoplastic peroxidases in the chitosaccharide-induced immediate oxidative burst and cytosolic Ca2+ increase in tobacco suspension culture. Plant Peroxid Newsl 14:117–124

    Google Scholar 

  • Kawano T, Kawano N, Hosoya H, Lapeyrie F (2001a) Fungal auxin antagonist hypaphorine competitively inhibits indole-3-acetic acid-dependent superoxide generation by horseradish peroxidase. Biochem Biophys Res Commun 288:546–551

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Kawano N, Muto S, Lapeyrie F (2001b) Cation-induced superoxide generation in tobacco cell suspension culture is dependent on ion valence. Plant Cell Environ 24:1235–1241

    Article  CAS  Google Scholar 

  • Kawano T, Kawano N, Lapeyrie F (2002a) A fungal auxin antagonist, hypaphorine prevents the indole-3-acetic acid-dependent irreversible inactivation of horseradish peroxidase: inhibition of Compound III-mediated formation of P-670. Biochem Biophys Res Commun 294:553–559

    Article  PubMed  Google Scholar 

  • Kawano T, Kawano N, Muto S, Lapeyrie F (2002b) Retardation and inhibition of the cation-induced superoxide generation in BY-2 tobacco cell suspension culture by Zn2+ and Mn2+. Physiol Plant 114:395–404

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Muto S, Adachi M, Hosoya H, Lapeyrie F (2002c) Spectroscopic evidence in support of horseradish peroxidase Compound II-catalyzed oxidation of salicylic acid but not of phenylethylamine. Biosci Biotechnol Biochem 66:651–654

    CAS  PubMed  Google Scholar 

  • Kawano T, Pinontoan R, Hosoya H, Muto S (2002d) Monoamine-dependent production of reactive oxygen species catalyzed by pseudoperoxidase activity of human hemoglobin. Biosci Biotechnol Biochem 66:1224–1232

    CAS  PubMed  Google Scholar 

  • Kawano T, Muto S, Adachi M, Hosoya H, Lapeyrie F (2002e) Spectroscopic evidence that salicylic acid converts a temporal inactive form of horseradish peroxidase (Compound III) to the irreversibly inactivated verdohemoprotein (P-670). Biosci Biotechnol Biochem 66:646–650

    CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2002) Ubiquitination and auxin signaling: a degrading story. Plant Cell S81-S95

    Google Scholar 

  • Kiba A, Toyota K, Ichinose Y, Yamada T, Shiraishi T (1996) Species-specific suppression of superoxide-anion generation of surfaces of pea leaves by the suppressor from Mycosphaella pinodes. Ann Phytopathol Soc Jpn 62:508–512

    CAS  Google Scholar 

  • Kiba A, Miyake C, Toyoda K, Ichinose Y, Yamada T, Shiraishi T (1997) Superoxide generation in extracts from isolated plant cell walls is regulated by fungal signal molecules. Phytopathology 87:843–852

    Google Scholar 

  • Kim YS, Min JK, Kim D, Jung J (2001) A soluble auxin-binding protein, ABP57: Purification with anti-bovine serum albumin antibody and characterization of its mechanistic role in the auxin effect on plant plasma membrane H+-ATPase. J Biol Chem 276:10730–10736

    CAS  PubMed  Google Scholar 

  • Krylov SN, Dunford HB (1996) Evidence for a free radical chain mechanism in the reaction between peroxidase and indole-3-acetic acid at neutral pH. Biophys Chem 58:325–338

    Article  CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  Google Scholar 

  • Lee JS (1998) The mechanism of stomatal closing by salicylic acid in Commelina communis L. J Plant Biol 41:97–102

    Google Scholar 

  • Lee JS, Mulkey TJ, Evans ML (1983) Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 220:1375–1376

    Google Scholar 

  • Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Taylor ATS, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communi. Plant Physiol 121:147–152

    Article  CAS  PubMed  Google Scholar 

  • Luschni C, Fink GR (1999) Two pieces of the auxin puzzle. Trends Plant Sci 4:162–164

    Article  PubMed  Google Scholar 

  • Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073

    CAS  PubMed  Google Scholar 

  • Martin F, Lapeyrie F, Tagu D (1997) Altered gene expression during ectomycorrhizal development. In: Carrol, G, Tudzynski P (eds) The Mycota, vol 5, part A. Springer, Berlin Heidelberg New York, pp 139–196

  • Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42:1383–1388

    Article  CAS  PubMed  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1–1 and abi2–1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    Google Scholar 

  • Nehls U, Beguiristain T, Ditengou F, Lapeyrie F, Martin F (1998) The expression of a symbiosis-regulated gene in eucalypt roots is regulated by auxins and hypaphorine, the tryptophan betaine of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Planta 207:296–302

    Article  CAS  PubMed  Google Scholar 

  • Ohtani K, Ogawa K, Kasai R, Yang CR, Yamasaki K, Zhou J, Tanaka O (1992) Oleanane glycosides from Glycyrrhiza yunnanensis roots. Phytochemistry 31:1747–1752

    Article  CAS  PubMed  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxidase mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Google Scholar 

  • Pfeiffer W, Höftberger M (2001) Oxidative burst in Chenopodium rubrum suspension cells: induction by auxin and osmotic changes. Physiol Plant 111:144–150

    Article  CAS  Google Scholar 

  • Pinontoan R, Krystofava S, Kawano T, Mori IC, Tsuji T, Iida H, Muto S (2002) Phenylethylamine induces an increase in cytosolic Ca2+ in yeast. Biosci Biotechnol Biochem 66:1069–1074

    CAS  PubMed  Google Scholar 

  • Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310

    Google Scholar 

  • Raz V, Fluhr R (1992) Calcium requirement for ethylene-dependent responses. Plant Cell 4:1123–1130

    CAS  Google Scholar 

  • Reddy ASN, Koshiba T, Theologis A, Pouvaiah BW (1988) The effect of calcium antagonists on auxin-induced elongation and on the expression of two auxin-regulated genes on pea epicotyls. Plant Cell Physiol 29:1165–1170

    CAS  Google Scholar 

  • Rutter R, Valentine M, Hendrich MP, Hager LP, Debrunner PG (1983) Chemical nature of the porphyrin pi cation radical in horseradish peroxidase Compound I. Biochemistry 22:4769–4774

    CAS  PubMed  Google Scholar 

  • Sakurai N, Nevins DJ, Masuda Y (1977) Auxin- and hydrogen ion-induced cell wall loosening and cell extension in Avena coleoptile segments. Plant Cell Physiol 18:371–380

    CAS  Google Scholar 

  • Savitsky PA, Gazaryan IG, Tishkov VI, Lagrimini LM, RuzGas T, Gorton L (1999) Oxidation of indole-3-acetic acid by dioxygen catalyzed by plant peroxidases: specificity for the enzyme structure. Biochem J 340:579–583

    Article  CAS  PubMed  Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688

    Article  CAS  PubMed  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    Article  CAS  PubMed  Google Scholar 

  • Schulz CE, Rutter R, Sage JT, Debrunner PG, Hager LP (1984) Mossbauer and electron paramagnetic resonance studies of horseradish peroxidase and its catalytic intermediates. Biochemistry 23:4743–454

    CAS  PubMed  Google Scholar 

  • Schweikert C, Liszkay A, Schopfer P (2000) Scission of polysaccharides by peroxidase-generated hydroxy radicals. Phytochemistry 53:562–570

    Article  Google Scholar 

  • Takahama U, Yoshitama K (1998) Hydoxycinnamic acid esters enhance peroxidase-dependent oxidation of 3,4-dihydroxyphenylamine. Differences in the enhancement among the esters. J Plant Res 111:97–100

    CAS  Google Scholar 

  • Wandji J, Awanchiri SS, Fomum ZT, Tillequin F, Libot F (1995) Isoflavones and alkaloids from the stem bark and seeds of Erythrina senegalensis. Phytochemistry 39:677–681

    Article  CAS  Google Scholar 

  • White RF (1979) Acetylsalicylic acid induces resistance to tobacco mosaic virus in tobacco. Virology 99:410–412

    CAS  Google Scholar 

  • Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiol 115:1405–1412

    CAS  PubMed  Google Scholar 

  • Yoshioka H, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant Microbe Int 14:725–736

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Kawano.

Additional information

Communicated by P.P. Kumar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawano, T. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21, 829–837 (2003). https://doi.org/10.1007/s00299-003-0591-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-003-0591-z

Keywords

Navigation