Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean

Jun-Min He A C D , Hua Xu C , Xiao-Ping She C , Xi-Gui Song C and Wen-Ming Zhao A
+ Author Affiliations
- Author Affiliations

A Center of Bioinformation, School of Life Sciences and Technology,

B Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China.

C School of Life Sciences, Shaanxi Normal University, Xi’an 710062, People’s Republic of China.

D Corresponding author. Email: hejm1965@yahoo.com.cn

Functional Plant Biology 32(3) 237-247 https://doi.org/10.1071/FP04185
Submitted: 10 October 2004  Accepted: 10 February 2005   Published: 5 April 2005

Abstract

Previous studies have showed that UV-B can stimulate closure as well as opening of stomata. However, the mechanism of this complex effect of UV-B is not clear. The purpose of this paper is to investigate the role and the interrelationship of H2O2 and NO in UV-B-induced stomatal closure in broad bean (Vicia faba L.). By epidermal strip bioassay and laser-scanning confocal microscopy, we observed that UV-B-induced stomatal closure could be largely prevented not only by NO scavenger c-PTIO or NO synthase (NOS) inhibitor l-NAME, but also by ascorbic acid (ASC, an important reducing substrate for H2O2 removal) or catalase (CAT, the H2O2 scavenger), and that UV-B-induced NO and H2O2 production in guard cells preceded UV-B-induced stomatal closure. These results indicate that UV-B radiation induces stomatal closure by promoting NO and H2O2 production. In addition, c-PTIO, l-NAME, ASC and CAT treatments could effectively inhibit not only UV-B-induced NO production, but also UV-B-induced H2O2 production. Exogenous H2O2-induced NO production and stomatal closure were partly abolished by c-PTIO and l-NAME. Similarly, exogenous NO donor sodium nitroprusside-induced H2O2 production and stomatal closure were also partly reversed by ASC and CAT. These results show a causal and interdependent relationship between NO and H2O2 during UV-B-regulated stomatal movement. Furthermore, the l-NAME data also indicate that the NO in guard cells of Vicia faba is probably produced by a NOS-like enzyme.

Keywords: UV-B radiation, stomatal closure, nitric oxide, hydrogen peroxide, broad bean (Vicia faba L.).


References


Able AJ, Sutherland MW, Guest DI (2003) Production of reactive oxygen species during non-specific elicitation, non-host resistance and field resistance expression in cultured tobacco cells. Functional Plant Biology 30, 91–99.
CrossRef | open url image1

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

Allen GJ, Chu SP, Schumacher K, Shinmazaki CT, Vafeados D , et al. (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289, 2338–2342.
CrossRef | PubMed | open url image1

Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.
CrossRef | PubMed | open url image1

Ambasht NK, Agrawal M (1998) Physiological and biochemical responses of Sorghum vulgare plants to supplemental ultraviolet-B radiation. Canadian Journal of Botany 76, 1290–1294.
CrossRef | open url image1

Barceló AR, Pomar F, López-Serrano M, Pedreño MA (2003) Peroxidase: a multifunctional enzyme in grapevines. Functional Plant Biology 30, 577–591.
CrossRef | open url image1

Beligni MV, Lamattina L (1999) Is nitric oxide toxic or protective? Trends in Plant Science 4, 299–300.
CrossRef | PubMed | open url image1

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

Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. Journal of Experimental Botany 53, 1367–1376.
CrossRef | PubMed | open url image1

Caldwell, MM (1971). Solar ultraviolet radiation and the growth and development of higher plants. In ‘Photophysiology’. pp. 131–177. (Academic Press: New York)

Cathcart R, Schwiers E, Ames BN (1983) Detection of picomol levels of hydroperoxides using a fluorescent dichlorifluorescein assay. Analytical Biochemistry 134, 111–116.
CrossRef | PubMed | open url image1

Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension culture. The Plant Journal 24, 667–677.
CrossRef | PubMed | open url image1

Corpas FJ, Barroso JB, del Rio LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant. Trends in Plant Science 6, 145–150.
CrossRef | PubMed | open url image1

Cueto M, Hernandez-Perera O, Martin R, Bentura ML, Rodrigo J, Lamas S, Golvano MP (1996) Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Letters 398, 159–164.
CrossRef | PubMed | open url image1

Dangl J (1998) Innate immunity. Plants just say NO to pathogens. Nature 394, 525–527.
CrossRef | PubMed | open url image1

Dat J, Vandenbeele S, Vranova E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress response. Cellular and Molecular Life Sciences 57, 779–795.
CrossRef | PubMed | open url image1

Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide signal functions in plant disease resistance. Nature 394, 585–588.
CrossRef | PubMed | open url image1

Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 99, 16314–16318.
CrossRef | open url image1

Desikan R, Cheung M-K, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill S (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
CrossRef | open url image1

Dong FC, Wang PT, Zhang L, Song CP (2001) The role of hydrogen peroxide in salicylic acid-induced stomatal closure in Vicia faba guard cells. Acta Phytophysiologica Sinica 27, 296–302. open url image1

Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Current Opinion in Plant Biology 2, 369–374.
CrossRef | PubMed | open url image1

Eisinger WR, Swartz RE, Bogomolni RA, Taiz L (2000) The ultraviolet action spectrum for stomatal opening in broad bean. Plant Physiology 122, 99–105.
CrossRef | PubMed | open url image1

Eisinger WR, Bogomolni RA, Taiz L (2003) Interactions between a blue–green reversible photoreceptor and a separate UV-B receptor in stomatal guard cells. American Journal of Botany 90, 1560–1566. open url image1

Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. The Plant Journal 23, 817–824.
CrossRef | 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 | PubMed | open url image1

Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Physiologia Plantarum 100, 241–254.
CrossRef | open url image1

García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 126, 1196–1204.
CrossRef | PubMed | open url image1

García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiology 128, 790–792.
CrossRef | PubMed | open url image1

García-Mata C, Lamattina L (2003) Abscisic acid, nitric oxide and stomatal closure — is nitrate reductase one of the missing links? Trends in Plant Science 8, 20–26.
CrossRef | PubMed | open url image1

Giannini A, Pardossi A, Lercari B (1996) The use of UV radiation to control the architecture of Salvia splendens plants. 1. Effects on plant growth, water relations and gas exchange. Photochemistry and Photobiology 64, 123–130. open url image1

Grammatikopoulos G, Karabourniotis G, Kyparissis A, Petropoulou Y, Manetas Y (1994) Leaf hairs of olive (Olea europaea) prevent stomatal closure by ultraviolet-B radiation. Australian Journal of Plant Physiology 21, 293–301. open url image1

Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100–103.
CrossRef | PubMed | open url image1

He YK, Tang R-H, Hao Y, Stevens RD, Cook CW , et al. (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968–1971.
CrossRef | PubMed | open url image1

Hu X, Neill SJ, Cai W, Tang Z (2003) Nitric oxide mediates elicitor-induced saponin synthesis in cell cultures of Panax ginseng. Functional Plant Biology 30, 901–907.
CrossRef | open url image1

Jansen MAK, Noort REVD (2000) Ultraviolet-B radiation induces complex alterations in stomatal behaviour. Physiologia Plantarum 110, 189–194.
CrossRef | open url image1

Jordan BR (2002) Molecular response of plant cells to UV-B stress. Functional Plant Biology 29, 909–916.
CrossRef | open url image1

Kojima H, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, Tanaka J, Kudo Y, Nagano T (1998) Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. Neuroreport 9, 3345–3348.
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 | PubMed | open url image1

Lee S, Choi H, Suh S, Doo IS, Oh K-Y, Choi EJ, Taylor SAT, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduced stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiology 121, 147–152.
CrossRef | PubMed | open url image1

Li SS, Paulsson M, Bjorn LO (2002) Temperature-dependent formation and photorepair of DNA damage induced by UV-B radiation in suspension-cultured tobacco cells. Journal of Photochemistry and Photobiology. B, Biology 66, 67–72.
CrossRef | PubMed | open url image1

Liu X, Zhang SQ, Lou CH (2003) Involvement of nitric oxide in the signal transduction of salicylic acid regulating stomatal movement. Chinese Science Bulletin 48, 449–452.
CrossRef | open url image1

Lum HK, Butt YKC, Lo SCL (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Paseolus aureus). Nitric Oxide 6, 205–213.
CrossRef | PubMed | open url image1

Mackerness SAH, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Letters 489, 237–242.
CrossRef | PubMed | open url image1

McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiology 111, 1031–1042.
PubMed |
open url image1

Musil CF, Wand SJE (1993) Responses of sclerophyllous Ericaceae to enhanced level of ultraviolet-B radiation. Environmental and Experimental Botany 33, 233–242.
CrossRef | open url image1

Neill SJ, Desikan R, Clarke A, Hancock JT (2002a) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiology 128, 13–16.
CrossRef | PubMed | open url image1

Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002b) Hydrogen peroxide and nitric oxide as signaling molecules in plants. Journal of Experimental Botany 53, 1237–1247.
CrossRef | PubMed | open url image1

Nogués S, Allen DJ, Morison JIL, Baker NR (1998) Ultraviolet-B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiology 117, 173–181.
CrossRef | PubMed | open url image1

Nogués S, Allen DJ, Morison JIL, Baker NR (1999) Characterization of stomatal closure caused by ultraviolet-B radiation. Plant Physiology 121, 489–496.
CrossRef | PubMed | open url image1

Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JL (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406, 731–734.
CrossRef | PubMed | open url image1

Scandalios JG (1993) Oxygen stress and superoxide dismutase. Plant Physiology 101, 7–12.
PubMed |
open url image1

Sen S, Cheema IR (1995) Nitric oxide synthase and calmodulin immunoreactivity in plant embryonic tissue. Biochemical Archives 11, 221–227. open url image1

Stapleton AE (1992) Ultraviolet radiation and plants: burning questions. The Plant Cell 4, 1353–1358.
CrossRef | PubMed | open url image1

Teramura AH, Tevini M, Iwanzik W (1983) Effects of ultraviolet-B irradiation on plants during mild water stress. 1. Effects on diurnal stomatal resistance. Physiologia Plantarum 57, 175–180. open url image1

Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Letters 468, 89–92.
CrossRef | PubMed | 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 | PubMed | open url image1

Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438–1448.
CrossRef | PubMed | open url image1

Zhao Z, Chen G, Zhang C (2001) Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Australian Journal of Plant Physiology 28, 1055–1061. open url image1








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