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Strboh A homologue of NADPH oxidase regulates wound-induced oxidative burst and facilitates wound-healing in potato tubers

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Abstract

During 30-months of storage at 4°C, potato (Solanum tuberosum L.) tubers progressively lose the ability to produce superoxide in response to wounding, resist microbial infection, and develop a suberized wound periderm. Using differentially aged tubers, we demonstrate that Strboh A is responsible for the wound-induced oxidative burst in potato and aging attenuates its expression. In vivo superoxide production and NADPH oxidase (NOX) activity from 1-month-old tubers increased to a maximum 18–24 h after wounding and then decreased to barely detectable levels by 72 h. Wounding also induced a 68% increase in microsomal protein within 18 h. These wound-induced responses were lost over a 25- to 30-month storage period. Superoxide production and NOX activity were inhibited by diphenylene iodonium chloride, a specific inhibitor of NOX, which in turn effectively inhibited wound-healing and increased susceptibility to microbial infection and decay in 1-month-old tubers. Wound-induced superoxide production was also inhibited by EGTA-mediated destabilization of membranes. The ability to restore superoxide production to EGTA-treated tissue with Ca+2 declined with advancing tuber age, likely a consequence of age-related changes in membrane architecture. Of the five homologues of NOX (Strboh A-D and F), wounding induced the expression of Strboh A in 6-month-old tubers but this response was absent in tubers stored for 25–30 months. Strboh A thus mediates the initial burst of superoxide in response to wounding of potato tubers; loss of its expression increases the susceptibility to microbial infection and contributes to the age-induced loss of wound-healing ability.

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Abbreviations

CaM:

Calmodulin

CL:

Chemiluminescence

DPI:

Diphenylene iodonium chloride

NOX:

NADPH oxidase

NBT:

Nitroblue tetrazolium

OB:

Oxidative burst

PAL:

Phenylalanine ammonia lyase

POX:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

References

  • Amicucci E, Gaschler K, Ward JM (1999) NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pondweed. Plant Biol 1:524–528

    CAS  Google Scholar 

  • Auh CK, Murphy TM (1995) Plasma membrane redox enzyme is involved in the synthesis of O2- and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol 107:1241–1247

    PubMed  CAS  Google Scholar 

  • Bernards MA, Fleming WD, Llewellyn DB, Priefer R, Yang X, Sabatino A, Plourde GL (1999) Biochemical characterization of the suberization-associated anionic peroxidase of potato. Plant Physiol 121:135–146

    Article  PubMed  CAS  Google Scholar 

  • Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30

    Article  PubMed  CAS  Google Scholar 

  • Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Peragon J, Contreras-Jurado C, García-Salguero L, Corpas FJ, Esteban FJ, Peinado MA, De La Higuera M, Lupianez JA (1998) Impact of starvation-refeeding on kinetics and protein expression of trout liver NADPH-production systems. Am J Physiol Regul Integr Comp Physiol 274:R1578–R1587

    CAS  Google Scholar 

  • Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence-a broad perspective. Physiol Mol Plant Path 51:347–366

    Article  CAS  Google Scholar 

  • Bolwell GP (1999) Role of active oxygen species and NO in plant defense responses. Curr Opinion Plant Biol 2:287–294

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Doke N (1983a) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissue infection with an incompatible race of Phytophthora infestans and the hypal wall components. Physiol Plant Path 23:345–357

    Article  CAS  Google Scholar 

  • Doke N (1983b) Generation of superoxide anion by potato tuber protoplasts upon the hypersensitive response to hypal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressor of hypersensitivity. Physiol Plant Pathol 23:359–367

    CAS  Google Scholar 

  • Doke N, Miura Y (1995) In-vitro activation of NADPH-dependent O2(-) generating-system in a plasma membrane-rich fraction of potato-tuber tissues by treatment with an elicitor from Phytophthora infestans or with digitonin. Physiol Mol Plant Path 46:17–28

    Article  CAS  Google Scholar 

  • Doke N, Ohashi Y (1988) Involvement of a superoxide generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol Mol Plant Path 32:63–175

    Article  Google Scholar 

  • Evensen KB (1984) Calcium effects on ethylene and ethane production and 1-aminocyclopropane-1-carboxylic acid content in potato disks. Physiol Plant 60:125–128

    Article  CAS  Google Scholar 

  • Furuichi N, Yokokawa K, Hatsugai N, Miyazaki Y (2001) Induction of plant NADPH oxydase homolog by 38 KD elicitor of Phytophthora infesans in potato. Direct submission (AB064343) to NCBI

  • Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21–29

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    Article  PubMed  CAS  Google Scholar 

  • Hancock JT, Desikan R, Clarke A, Hurst RD, Neill SJ (2002) Cell signaling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species. Plant Physiol Biochem 40:611–617

    Article  CAS  Google Scholar 

  • Johnson SM, Doherty SJ, Croy RRD (2003) Biphasic superoxide generation in potato tubers. A self-amplifying response to stress. Plant Physiol 131:1–10

    Article  CAS  Google Scholar 

  • Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca+2 binding domains. Plant Cell 10:255–266

    Article  PubMed  CAS  Google Scholar 

  • Knowles NR, Iritani WM, Weller LD, Gross DC (1982) Susceptibility of potatoes to bacterial rot and weight loss as a function of wound-healing and temperature. Am Potato J 59:515–522

    Google Scholar 

  • Knowles NR, Knowles LO (1989) Correlations between electrolyte leakage and degree of saturation of polar lipids from aged potato (Solanum tuberosum L) tuber tissue. Ann Bot 63:331–338

    Google Scholar 

  • Kobayashi M, Kawakita K, Maeshima M, Doke N, Yoshioka H (2006) Subcellular localization of Strboh proteins and NADPH-dependent O2(−)-generating activity in potato tuber tissues. J Exp Bot 57:1373–1379

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokata N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    Article  PubMed  CAS  Google Scholar 

  • Konze JR, Elstner EF (1978) Ethane and ethylene formation by mitochondria as indication of aerobic lipid degradation in response to wounding of plant tissue. Biochim Biophys Acta 528:213–221

    PubMed  CAS  Google Scholar 

  • Kumar GNM, Knowles NR (1993a) Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed-tubers. Plant Physiol 102:115–124

    PubMed  CAS  Google Scholar 

  • Kumar GNM, Knowles NR (1993b) Age of potato seed-tubers influences protein synthesis during sprouting. Physiol Plant 89:262–270

    Article  CAS  Google Scholar 

  • Kumar GNM, Knowles NR (1996) Oxidative stress results in increased sinks for metabolic energy during aging and sprouting of potato seed-tubers. Plant Physiol 112:1301–1313

    PubMed  CAS  Google Scholar 

  • Kumar GNM, Houtz RL, Knowles NR (1999) Age-induced protein modifications and increased proteolysis in potato seed-tubers. Plant Physiol 119:89–99

    Article  PubMed  CAS  Google Scholar 

  • Kumar GNM, Knowles NR (2003) Wound-induced superoxide production and PAL activity decline with potato seed-tuber age and wound-healing ability. Physiol Plant 117:108–117

    Article  CAS  Google Scholar 

  • Kumar GNM, Iyer S, Knowles NR (2007) Extraction of RNA from frozen and lyophilized tuber and root tissues. J Agric Food Chem 55:1674–1678

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  PubMed  CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    Article  PubMed  CAS  Google Scholar 

  • Leavey PJ, Gonzalez-Aller C, Thruman G, Kleinberg M, Rinckel L, Ambruso DW, Freeman S, Kuypers FA, Ambruso DR (2002) A 29-kDa protein associated with p67phox expresses both peroxyredoxin and phospholipase A2 activity and enhances superoxide anion production by a cell-free system of NADPH oxidase activity. J Biol Chem 277:45181–45187

    Article  PubMed  CAS  Google Scholar 

  • Leusen JHW, Verhoeven AJ, Roos D (1996) Interactions between the components of the human NADPH oxidase: a review about the intrigues in the phox family. Frontiers Biosci 1:d72–d90

    CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  CAS  Google Scholar 

  • Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496

    Article  PubMed  CAS  Google Scholar 

  • Liu HT, Sun DY, Zhou RG (2005) Ca2+ and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell Environ 28:1276–1284

    Article  CAS  Google Scholar 

  • Li LL, Dinauer MC (1998) Reconstitution of NADPH oxidase activity in human X-linked chronic granulomatous disease myeloid cells after stable gene transfer using a recombinant adeno-associated virus 2 vector. Blood cells Mol Dis 15:522–538

    Article  Google Scholar 

  • Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139:935–948

    Article  PubMed  CAS  Google Scholar 

  • Lulai EC, Orr PH (1994) Techniques for detecting and measuring developmental and maturational changes in tuber native periderm. Am Potato J 71:489–505

    Google Scholar 

  • Lulai EC, Orr PH (1995) Porometric measurements indicate wound severity and tuber maturity affects the early stages of wound-healing. Am Potato J 72:225–241

    Google Scholar 

  • Lulai EC, Corsini DL (1998) Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiol Mol Plant Path 53:209–222

    Article  CAS  Google Scholar 

  • Matsuda F, Morino K, Miyashita M, Miyagawa H (2003) Metabolic flux analysis of the phenylpropanoid pathway in wound-healing potato tuber tissue using stable isotope-labeled tracer and LC-MS spectroscopy. Plant Cell Physiol 44:510–517

    Article  PubMed  CAS  Google Scholar 

  • Miura Y, Yoshioka H, Doke N (1995) An autophotographic determination of the active oxygen generation in potato tuber discs during hypersensitive response to fungal infection or elicitor. Plant Sci 105:45–52

    Article  CAS  Google Scholar 

  • Park HJ, Miura Y, Kawakita K, Yoshioka H, Doke N (1998) Physiological mechanisms of a sub-systemic oxidative burst triggered by elicitor-induced local oxidative burst in potato tuber slices. Plant Cell Physiol 39(11):1218–1225

    CAS  Google Scholar 

  • Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasmamembrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077–2091

    Article  PubMed  CAS  Google Scholar 

  • Razem FA, Bernards MA (2003) Reactive oxygen species production with suberization: evidence for an NADPH-dependent oxidase. J Exp Bot 54:935–941

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004a) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004b) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628

    Article  PubMed  CAS  Google Scholar 

  • Simon-Plas F, Elmayan T, Blein JP (2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J 31:137–147

    Article  PubMed  CAS  Google Scholar 

  • Stuehr DJ, Fasehun OA, Kwon NS (1991) Inhibition of macrophage and endothelial cell nitric oxide synthase by diphenyleneiodonium and its analogs. FASEB J 5:98–103

    PubMed  CAS  Google Scholar 

  • Taylor MA, Wright F, Davies HV (1994) Characterization of the cDNA clones of two beta-tubulin genes and their expression in the potato plant (Solanum tuberosum L.). Plant Mol Biol 26:1013–1018

    Article  PubMed  CAS  Google Scholar 

  • Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci USA 92:4158–4163

    Article  PubMed  CAS  Google Scholar 

  • Tian WN, Braunstein LD, Apse K, Pang J, Rose M, Tian X, Stanton RC (1999) Importance of glucose-6-phosphate dehydrogenase activity in cell death. Am J Physiol 276:C1121–C1131

    PubMed  CAS  Google Scholar 

  • Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J 14:365–370

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134

    Article  PubMed  CAS  Google Scholar 

  • Van Gestelen P, Asard H, Horemans N, Caubergs RJ (1998) Superoxide-producing NAD(P)H oxidases in plasma membrane vesicles from elicitor responsive bean plants. Physiol Plant 104:653–660

    Article  Google Scholar 

  • Vogt E, Schonher J, Schmidt HW (1983) Water permeability of periderm membranes isolated enzymatically from potato tubers (Solanum tuberosum L.). Planta 158:294–301

    Article  CAS  Google Scholar 

  • Yamamizo C, Kuchimura K, Kobayashi A, Katou S, Kawakita K, Jones JD, Doke N, Yoshioka H (2006) Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol 140:681–692

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka H, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp 91 phox homologue by fungal cell wall, arachidonic acid, and salicylic acid in potato. MPMI 14:725–736

    PubMed  CAS  Google Scholar 

  • Zabrouskov V, Knowles NR (2002a) Lipid metabolism during aging of high α-linolenate-phenotype potato tubers. Arch Biochem Biophys 402:136–148

    Article  PubMed  CAS  Google Scholar 

  • Zabrouskov V, Knowles NR (2002b) Changes in lipid molecular species and sterols of microsomal membranes during aging of potato (Solanum tuberosum L.) seed-tubers. Lipids 37:309–315

    Article  PubMed  CAS  Google Scholar 

  • Zabrouskov V, Kumar GNM, Spychalla JP, Knowles NR (2002) Oxidative metabolism and the physiological age of seed potatoes are affected by increased alpha-linolenate content. Physiol Plant 116(2):172–185

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the USDA/ARS (project no. 11D-3055-5461) and the Agricultural Research Center, Washington State University.

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  1. Postharvest Physiology and Biochemistry Laboratory, Department of Horticulture and Landscape Architecture, Washington State University, P.O. Box 646414, Pullman, WA, 99164-6414, USA

    G. N. Mohan Kumar, Suresh Iyer & N. Richard Knowles

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  1. G. N. Mohan Kumar
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Correspondence to N. Richard Knowles.

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Kumar, G.N.M., Iyer, S. & Knowles, N.R. Strboh A homologue of NADPH oxidase regulates wound-induced oxidative burst and facilitates wound-healing in potato tubers. Planta 227, 25–36 (2007). https://doi.org/10.1007/s00425-007-0589-9

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