Copper amine oxidase-catalysed hydrogen peroxide involves production of nitric oxide in darkness-induced stomatal closure in broad bean
Ai-Xia Huang A , Yong-Shun Wang A , Xiao-Ping She A B , Juan Mu A and Jin-Liang Zhao A
+ Author Affiliations
- Author Affiliations
A College of Life Sciences, Shaanxi Normal University, Xi’an 710062, China.
B Corresponding author. Email: shexiaoping@snnu.edu.cn
Functional Plant Biology 42(11) 1057-1067 https://doi.org/10.1071/FP15172
Submitted: 18 June 2015 Accepted: 21 August 2015 Published: 30 September 2015
Abstract
Hydrogen peroxide is an important intermediate in darkness-induced stomatal closure. In the present work, we provide evidence that copper amine oxidase (CuAO) was involved in H2O2 production in darkness-induced stomatal closure in Vicia faba L. Darkness activated CuAO in intercellular washing fluid from leaves. Aminoguanidine (AG) and 2-bromoethylamine (BEA), which were both irreversible inhibitors of CuAO, significantly suppressed darkness-induced stomatal closure and H2O2 generation. The effects of AG and BEA were reversed only by H2O2 but not by other products of CuAO. These results indicate that CuAO participates in darkness-induced stomatal closure through its reaction product, H2O2. Furthermore, darkness-induced nitric oxide (NO) production and cytosolic alkalinisation were obviously inhibited by AG and BEA, and only H2O2, among the products of CuAO, could reverse the effects, implying that the CuAO-catalysed product H2O2 is required for NO production and cytosolic alkalinisation to a large extent in darkness-induced stomatal closure. In addition, butyric acid blocked but methylamine enhanced the ability of H2O2 to reverse the effect of BEA on NO production, suggesting that cytosolic alkalinisation is involved in CuAO-mediated NO generation in darkness-induced stomatal closure.
Additional keywords: 2-bromoethylamine, aminoguanidine, stomatal movement, Vicia faba.
References
Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. The Plant Cell 9, 1559–1572.| Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsFeltL8%3D&md5=97b71a338f679faf73c04339f7e00220CAS | 12237396PubMed |
An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. Journal of Experimental Botany 59, 815–825.
| Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1Khtbo%3D&md5=6e6c35d70e6b311a95bfc6e2330a9ca5CAS | 18272918PubMed |
Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiologia Plantarum 104, 195–202.
| Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFSrsbY%3D&md5=783f31667340e159bf0282f263a72728CAS |
Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20, 301–317.
| Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1Gjsrc%3D&md5=5f360a47ff3eea84115c8a7efba6ced7CAS | 11354606PubMed |
Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219, 847–855.
| Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1Glurc%3D&md5=89755c260b7c43e9b6ed2478afecf339CAS | 15133666PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=0c5b9be40df67b5bda977fd44a3222a3CAS | 942051PubMed |
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal 45, 113–122.
| ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFOntw%3D%3D&md5=9636abcd5602c4742c0bde75c35ed50eCAS | 16367958PubMed |
Cona A, Cenci F, Cervelli M, Federico R, Mariottini P, Moreno S, Angelini R (2003) Polyamine oxidase, a hydrogen peroxide-producing enzyme, is up-regulated by light and down-regulated by auxin in the outer tissues of the maize mesocotyl. Plant Physiology 131, 803–813.
| Polyamine oxidase, a hydrogen peroxide-producing enzyme, is up-regulated by light and down-regulated by auxin in the outer tissues of the maize mesocotyl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjsLg%3D&md5=8349e0a60e5967711b40a802c6594512CAS | 12586904PubMed |
Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Function of amine oxidases in plant development and defence. Trends in Plant Science 11, 80–88.
| Function of amine oxidases in plant development and defence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFOjurs%3D&md5=4bf7a64677b30bb6342e25945030366aCAS | 16406305PubMed |
Desikan R, Cheung M-K, Bright J, Henson D, Hancock JT, Neill SJ (2004a) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. Journal of Experimental Botany 55, 205–212.
| ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslaq&md5=665eac2a288e2cf80034b031c4ad4c2dCAS | 14673026PubMed |
Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R, Rock C (2004b) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
| Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsleltbs%3D&md5=f78c3b42236a84ae3c7ae7038d24a856CAS |
Gonugunta VK, Srivastava N, Puli MR, Raghavendra AS (2008) Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid. Plant, Cell & Environment 31, 1717–1724.
| Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtl2hs7zN&md5=7dc6ce17ac790cda2067aac8b621e08fCAS |
Gonugunta VK, Srivastava N, Raghavendra AS (2009) Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan. Plant Signaling & Behavior 4, 561–564.
| Cytosolic alkalinization is a common and early messenger preceding the production of ROS and NO during stomatal closure by variable signals, including abscisic acid, methyl jasmonate and chitosan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFelurk%3D&md5=bd11cc1ec0d9fb6bcd5273cbcd8eeb41CAS |
He J, Yue X, Wang R, Zhang Y (2011) Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L. Journal of Experimental Botany 62, 2657–2666.
| Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVyksL8%3D&md5=358bbae143337787fad35a56380412f5CAS | 21212297PubMed |
Huang AX, She XP, Huang C, Song TS (2007) The dynamic distribution of NO and NADPH–diaphorase activity during IBA-induced adventitious root formation. Physiologia Plantarum 130, 240–249.
| The dynamic distribution of NO and NADPH–diaphorase activity during IBA-induced adventitious root formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslOhtLo%3D&md5=b8432e361c402f3caf85cd0e2a593e38CAS |
Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proceedings of the National Academy of Sciences of the United States of America 89, 1790–1794.
| Changes in cytosolic pH and calcium of guard cells precede stomatal movements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xitlaitb0%3D&md5=ca8e9dd37eee2e7dad8fb8f73e2debe3CAS | 11607281PubMed |
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.
| Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotV2ktrc%3D&md5=f905b9830f7aaaa3e0ec10725d379e07CAS | 9855277PubMed |
Kopyra M, Gwozdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiology and Biochemistry 41, 1011–1017.
| Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlyluro%3D&md5=4d23ff157f1e9289f6d8ef10de7f6217CAS |
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228, 367–381.
| Polyamines: essential factors for growth and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVCjsb8%3D&md5=ed87d2fb6d071f8628ad8654055488b0CAS | 18594857PubMed |
Li JH, Liu YQ, Lü P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiology 150, 114–124.
| A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsr0%3D&md5=d6babfeef1b694c2fc9a743d0e62c195CAS | 19321706PubMed |
Liu X, Shi WL, Zhang SQ, Lou CH (2005) Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L. Chinese Science Bulletin 50, 520–525.
Liu J, Liu GH, Hou LX, Liu X (2010) Ethylene-induced nitric oxide production and stomatal closure in Arabidopsis thaliana depending on changes in cytosolic pH. Chinese Science Bulletin 55, 2403–2409.
| Ethylene-induced nitric oxide production and stomatal closure in Arabidopsis thaliana depending on changes in cytosolic pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFensLg%3D&md5=c771ba2e18b7ded8618eb5ef6543a89cCAS |
Lum HK, Butt YKC, Lo SCL (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide 6, 205–213.
| Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslyhtr8%3D&md5=41fa336cd258f9d07d40e05ca7b3bae6CAS | 11890745PubMed |
Ma YL, She XP, Yang SS (2013) Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba. Canadian Journal of Plant Science 93, 119–130.
| Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivVSru74%3D&md5=aafdad791ced8b50fa66e9e7d319692fCAS |
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.
Medda R, Padiglia A, Pedersen JZ, Agrò AF, Rotilio G, Floris G (1997) Inhibition of copper amine oxidase by haloamines: a killer product mechanism. Biochemistry 36, 2595–2602.
| Inhibition of copper amine oxidase by haloamines: a killer product mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsVSlurY%3D&md5=cba88f340f6beb17f570900fd680646bCAS | 9054566PubMed |
Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonzalez-Guzman M, Rodriguez PL, Schroeder JI, Broschè M, Kollist H (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiology 162, 1652–1668.
| PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCmtLbF&md5=0bf8faadf8d37c189a345c67398c387eCAS | 23703845PubMed |
Neill SJ, Desikan R, Hancock JT (2002a) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
| Hydrogen peroxide signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtlGjtL8%3D&md5=40cbf7a8c1e7883ac954b334ab324c50CAS |
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, 1237–1247.
| Hydrogen peroxide and nitric oxide as signalling molecules in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSls70%3D&md5=2bba10cb1edbe975bb029dd693a46331CAS | 11997372PubMed |
Nilsson BO (1999) Biological effects of aminoguanidine: an update. Inflammation Research 48, 509–515.
| Biological effects of aminoguanidine: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvF2msb8%3D&md5=8b9b7567a56831874a10986b4481b4f4CAS | 10563466PubMed |
Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiology 128, 865–875.
| Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1GqtrY%3D&md5=49cb550247653268eca8a2c8757f4290CAS | 11891243PubMed |
Rea G, De Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, De Gara L, Federico R, Angelini R, Tavladoraki P (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiology 134, 1414–1426.
| Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKms78%3D&md5=5a52742eb2f33e2379747cc5ed1ad134CAS | 15064377PubMed |
Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiology 150, 229–243.
| Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium.Crossref | GoogleScholarGoogle Scholar | 19279198PubMed |
Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiology 166, 2065–2076.
| Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure.Crossref | GoogleScholarGoogle Scholar | 25266633PubMed |
She XP, Song XG, He JM (2004) Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Botanica Sinica 46, 1292–1300.
Su GX, An ZF, Zhang WH, Liu Y (2005) Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. Journal of Plant Physiology 162, 1297–1303.
| Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCjuro%3D&md5=b3cbdc94f2c611279ca2d348745134dcCAS |
Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. Journal of Integrative Plant Biology 48, 426–432.
| Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFSqurk%3D&md5=f0cca174f984b23c046ec9a57ee699b0CAS |
Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiology 134, 1536–1545.
| Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmsLw%3D&md5=dd821d62558663a8af133a70287e0f90CAS | 15064385PubMed |
Tossi V, Lamattina L, Jenkins GI, Cassia RO (2014) Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV RESISTANCE LOCUS8 photoreceptor in a nitric oxide-dependent mechanism. Plant Physiology 164, 2220–2230.
| Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV RESISTANCE LOCUS8 photoreceptor in a nitric oxide-dependent mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2jtrk%3D&md5=981738bfa11c4dbf701dc32c21175cbcCAS | 24586043PubMed |
Wang Y, Chen ZH, Zhang B, Hills A, Blatt MR (2013) PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl– channels through reactive oxygen species-mediated sctivation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells. Plant Physiology 163, 566–577.
| PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl– channels through reactive oxygen species-mediated sctivation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Ojs7bF&md5=bc23851239c6f02ce34d56c341f9ffabCAS | 23899646PubMed |
Xie Y, Mao Y, Zhang W, Lai D, Wang Q, Shen W (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiology 165, 759–773.
| Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVWnurbI&md5=5caa9000c7dd8bb7e05739da5a47f24dCAS | 24733882PubMed |
Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiology 132, 1973–1981.
| Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVantL8%3D&md5=c91013304ce1dd7c14bca92053a80409CAS | 12913153PubMed |
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438–1448.
| Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFOjuro%3D&md5=acc3abad887ab474c5a4bf7d1800390bCAS | 11500543PubMed |
