Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP04035
RESEARCH ARTICLE
Contents Vol 31(9)

Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum

Radhika Desikan A , Man-Kim Cheung A , Andrew Clarke A , Sarah Golding A , Moshe Sagi B , Robert Fluhr C , Christopher Rock D , John Hancock A and Steven Neill A E
+ Author Affiliations
- Author Affiliations

A Centre for Research in Plant Science, Genomics Research Institute, Faculty of Applied Sciences, University of the West of England, Bristol, Coldharbour Lane, Bristol BS16 1QY, UK.

B The Institutes for Applied Research, PO Box 653, Beer Sheava 84105, Israel.

C Department of Plant Science, Weizmann Institute of Science, PO Box 26, Rehovot 76100, Israel.

D Department of Biological Sciences, Texas Tech University, PO Box 43131, Lubbock, TX 79409, USA.

E Corresponding author; email: steven.neill@uwe.ac.uk

Functional Plant Biology 31(9) 913-920 https://doi.org/10.1071/FP04035
Submitted: 14 February 2004  Accepted: 2 June 2004   Published: 27 September 2004

Abstract

The requirement for hydrogen peroxide (H2O2) generation and action during stomatal closure induced by darkness and abscisic acid (ABA) was investigated in pea (Pisum sativum L.). Stomatal closure induced by darkness or ABA was inhibited by the H2O2-scavenging enzyme catalase or the antioxidant N-acetyl cysteine (NAC), or by diphenylene iodonium (DPI), an inhibitor of the H2O2-generating enzyme NADPH oxidase. Exogenous H2O2 induced stomatal closure in a dose- and time-dependent manner, and H2O2 was also required for ABA-inhibition of stomatal opening in the light. H2O2 accumulation in guard cells was increased by darkness or ABA, as assessed with the fluorescent dye dichlorodihydrofluorescein diacetate (H2-DCFDA) and confocal microscopy. Such increases were inhibited by catalase, NAC or DPI, consistent with the effects of these compounds on stomatal apertures. Employing polymerase chain reaction (PCR) with degenerate oligonucleotide primers, several NADPH oxidase homologues were identified from pea genomic DNA that had substantial identity to the Arabidopsis thaliana (L.) Heynh. rboh (respiratory burst oxidase homologue) genes. Furthermore, an antibody raised against the tomato rboh identified immunoreactive proteins in epidermal, mesophyll and guard cells.

Keywords: abscisic acid, darkness, diphenylene iodonium, guard cells, hydrogen peroxide, NADPH oxidase.


Acknowledgments

Research in the UWE, Bristol laboratory is supported by the Leverhulme Trust and the BBSRC.


References


Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. The Plant Cell 9, 1559–1572.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Amicucci E, Gaschler K, Ward JM (1999) NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pond-weed (Potamogeton crispus). Plant Biology 1, 524–528. open url image1

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 Research 33, 531–545.
| PubMed |
open url image1

Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Current Opinion in Plant Biology 2, 287–294.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Burnett EC, Desikan R, Moser RC, Neill SJ (2000) ABA-induced MAP kinase activation in Pisum sativum peels correlates with stomatal responses to ABA. Journal of Experimental Botany 51, 197–205.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cross AR, Jones OTG (1986) The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Biochemical Journal 237, 111–116.
| PubMed |
open url image1

Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H , et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ, Jones JDG (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. The Plant Journal 10, 515–522.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guan L, Scandalios JG (1998) Effects of the plant growth regulator abscisic acid and high osmoticum on the developmental expression of the maize catalase genes. Physiologia Plantarum 104, 413–422.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Guan LM, 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. The Plant Journal 22, 87–95.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Havir EA (1992) The in vivo and in vitro inhibition of catalase from leaves of Nicotiana sylvestris by 3-amino-1,2,4-triazole. Plant Physiology 99, 533–537. open url image1

Hetherington AM (2001) Guard cell signalling. Cell 107, 711–714.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hey SJ, Bacon A, Burnett E, Neill SJ (1997) Abscisic acid signal transduction in epidermal cells of Pisum sativum L. Argenteum: both dehydrin mRNA accumulation and stomatal responses require protein phosphorylation and dephosphorylation. Planta 202, 85–92.
| Crossref | GoogleScholarGoogle Scholar | open url image1

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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiology 126, 1055–1060.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 Journal 22, 2623–2633.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee S, Choi H, Suh S, Doo I-S, Oh K-Y, 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 communis. Plant Physiology 121, 147–152.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lodhi MA, Guang-Ning Y, Weeden NF, Reisch BI (1994) A simple and efficient method for DNA extraction from grapevine cultivars, Vitis species and Ampelopsis. Plant Molecular Biology Reporter 12, 6–13. open url image1

Murata Y, Pei Z-M, 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. The Plant Cell 13, 2513–2523.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Neill SJ, Desikan R, Hancock JT (2002a) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany 53, 1237–1242.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 34, 187–203.
| PubMed |
open url image1

Prasad TK, Anderson MD, Stewart CR (1994) Acclimation, hydrogen peroxide and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology 105, 619–627.
| PubMed |
open url image1

Royer-Pokora B, Kunkel LM, Monaco AP, Goff SC, Newberger PE, Baehner RL, Cole FS, Curnutte JT, Orkin SH (1986) Cloning the gene for the inherited human disorder chronic granulomatous disease on the basis of its chromosomal location. Nature 322, 32–38.
| PubMed |
open url image1

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 Physiology 126, 1281–1290.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627–658.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Segal AW, Abo A (1993) The biochemical basis of the NADPH oxidase of phagocytes. Trends in Biochemical Sciences 18, 43–47.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Simon-Plas F, Elmayan T, Blein J-P (2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. The Plant Journal 31, 137–147.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JDG (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91-phox). The Plant Journal 14, 365–370.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences USA 99, 517–522.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Yoshioka H, Sugie K, Park H-J, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Molecular Plant–Microbe Interactions 14, 725–736. open url image1

Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JDG, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell 15, 706–718.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 Physiology 126, 1438–1448.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1