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Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves

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Abstract

The histochemical and cytochemical localization of abscisic acid (ABA)-induced H2O2 production in leaves of maize (Zea mays L.) plants were examined, using 3,3-diaminobenzidine (DAB) and CeCl3 staining, respectively, and the relationship between ABA-induced H2O2 production and ABA-induced subcellular activities of antioxidant enzymes was studied. H2O2 generated in response to ABA treatment was detected within 0.5 h in major veins of the leaves and maximized at about 2–4 h. In mesophyll and bundle sheath cells, ABA-induced H2O2 accumulation was observed only in apoplast, and the greatest accumulation occurred in the walls of mesophyll cells facing large intercellular spaces. Meanwhile, ABA treatment led to a significant increase in the activities of the leaf chloroplastic and cytosolic antioxidant enzymes superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR), and pretreatment with the NADPH oxidase inhibitor diphenyleneiodonium (DPI), the O 2 scavenger Tiron and the H2O2 scavenger dimethylthiourea (DMTU) almost completely arrested the increase in the activities of these antioxidant enzymes. Our results indicate that the accumulation of apoplastic H2O2 is involved in the induction of the chloroplastic and cytosolic antioxidant enzymes. Moreover, an oxidative stress induced by paraquat (PQ), which generates O 2 and then H2O2 in chloroplasts, also up-regulated the activities of the chloroplastic and cytosolic antioxidant enzymes, and the up-regulation was blocked by the pretreatment with Tiron and DMTU. These data suggest that H2O2 produced at a specific cellular site could coordinate the activities of antioxidant enzymes in different subcellular compartments.

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Abbreviations

ABA:

Abscisic acid

APX:

Ascorbate peroxidase

CAT:

Catalase

DAB:

3,3-diaminobenzidine

DMTU:

Dimethylthiourea

DPI:

Diphenyleneiodonium chloride

GR:

Glutathione reductase

NBT:

Nitro blue tetrazolium

PQ:

Paraquat

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Tiron:

1,2-dihydroxybenzene- 3,5-disulphonic acid

References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in contolling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  PubMed  CAS  Google Scholar 

  • Avsian-Kretchmer O, Gueta-Dahan Y, Lev-Yadun S, Gollop R, Ben-Hayyim G (2004) The salt-stress signal transduction pathway that activates the gpx1 promoter is mediated by intracellular H2O2, different from the pathway induced by extracellular H2O2. Plant Physiol 135:1685–1696

    Article  PubMed  CAS  Google Scholar 

  • Bellaire BA, Carmody J, Braud J, Gossett DR, Banks SW, Lucas MC, Fowler TE (2000) Involvement of abscisic acid-dependent and -independent pathways in the upregulation of antioxidant enzyme activity during NaCl stress in cotton callus tissue. Free Radical Res 33:531–545

    Article  CAS  Google Scholar 

  • Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209–221

    Article  PubMed  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 

  • Bueno P, Piqueras A, Kurepa J, Savouré A, Verbruggen N, Van Montagu M, Inzé D (1998) Expression of antioxidant enzymes in response to abscisic acid and high osmoticum in tobacco BY-2 cell cultures. Plant Sci 138:27–34

    Article  CAS  Google Scholar 

  • Desikan R, Cheung M-K, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill SJ (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Funct Plant Biol 31:913–920

    Article  CAS  Google Scholar 

  • Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037

    PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–45

    PubMed  CAS  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    Article  PubMed  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314

    PubMed  CAS  Google Scholar 

  • Guan L, Scandalios JG (1998) Two structurally similar maize cytosolic superoxide dismutase genes, Sod4 and Sod4A, respond differentially to abscisic acid and high osmoticum. Plant Physiol 117:217–224

    Article  PubMed  CAS  Google Scholar 

  • Guan L, Zhao J, Scandalios JG (2000) Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (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

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2002a) 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  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2002b) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2003) Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defense in leaves of maize seedlings. Plant Cell Environ 26:929–939

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2004) Abscisic acid and antioxidant defense in plant cells. Acta Bot Sin 46:1–9

    CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei Z-M, 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 

  • Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld J-P (2004) The Arabidopsis cytosolic h5 gene induction by oxidative stress and its w-box-mediated response to pathogen elicitor. Plant Physiol 134:1006–1016

    Article  PubMed  CAS  Google Scholar 

  • Lin CC, Kao CH (2001) Abscisic acid induced changes in cell wall peroxidase activity and hydrogen peroxide level in roots of rice seedlings. Plant Sci 160:323–329

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Alegre L (2003) Drought-induced changes in the redox state of α-tocopherol, ascorbate, and the diterpene carnosic acid in chloroplasts of Labiatae species differing in carnosic acid contents. Plant Physiol 131:1816–1825

    Article  PubMed  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder JI (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

    Article  PubMed  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 

  • Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cárdenas ML, Ryan C (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557

    Article  PubMed  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    Article  PubMed  Google Scholar 

  • Park SY, Ryu SH, Jang IC, Kwon SY, Kim JG, Kwak SS (2004) Molecular cloning of a cytosolic ascorbate peroxidase cDNA from cell cultures of sweetpotato and its expression in response to stress. Mol Genet Genomics 271:339–346

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  PubMed  CAS  Google Scholar 

  • Pastori G, Foyer CH, Mullineaux P (2000) Low temoerature-induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. J Exp Bot 51:107–113

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pellinen R, Palva T, Kangasjärvi J (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356

    Article  PubMed  CAS  Google Scholar 

  • Pellinen RI, Korhonen M-S, Tauriainen AA, Palva TP, Kangasjärvi J (2002) Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol 130:549–560

    Article  PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O 2 and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134

    Article  CAS  Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  PubMed  Google Scholar 

  • Yang G, Komatsu S (2000) Involvement of calcium-dependent protein kinase in rice (Oryza sativa L.) lamina inclination caused by brassinolide. Plant Cell Physiol 41:1243–1250

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for grants obtained from the Major State Basic Research Program of China (grant no. 2003CB114302), the National Natural Science Foundation of China (grant no. 30471048), the Key Project of Chinese Ministry of Education (grant no. 104100), and the Science Foundation of Doctoral Subject Point of Chinese Ministry of Education (grant no. 20040307011).

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Correspondence to Mingyi Jiang.

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Hu, X., Jiang, M., Zhang, A. et al. Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223, 57–68 (2005). https://doi.org/10.1007/s00425-005-0068-0

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