Skip to main content
SpringerLink
Log in

Copper amine oxidase and phospholipase D act independently in abscisic acid (ABA)-induced stomatal closure in Vicia faba and Arabidopsis

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Recent evidence has demonstrated that both copper amine oxidase (CuAO; EC 1.4.3.6) and phospholipase D (PLD; EC 3.1.4.4) are involved in abscisic acid (ABA)-induced stomatal closure. In this study, we investigated the interaction between CuAO and PLD in the ABA response. Pretreatment with either CuAO or PLD inhibitors alone or that with both additively led to impairment of ABA-induced H2O2 production and stomatal closure in Vicia faba. ABA-stimulated PLD activation could not be inhibited by the CuAO inhibitor, and CuAO activity was not affected by the PLD inhibitor. These data suggest that CuAO and PLD act independently in the ABA response. To further examine PLD and CuAO activities in ABA responses, we used the Arabidopsis mutants cuaoζ and pldα1. Ablation of guard cell-expressed CuAOζ or PLDα1 gene retarded ABA-induced H2O2 generation and stomatal closure. As a product of PLD, phosphatidic acid (PA) substantially enhanced H2O2 production and stomatal closure in wide type, pldα1, and cuaoζ. Moreover, putrescine (Put), a substrate of CuAO as well as an activator of PLD, induced H2O2 production and stomatal closure in WT but not in both mutants. These results suggest that CuAO and PLD act independently in ABA-induced stomatal closure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Acharya BR, Jeon BW, Zhang W, Assmann SM (2013) Open stomata 1 (OST1) is limiting in abscisic acid responses of Arabidopsis guard cells. New Phytol 200:1049–1063

    Article  CAS  PubMed  Google Scholar 

  • Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    Article  CAS  PubMed  Google Scholar 

  • 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. J Exp Bot 59:815–825

    Article  CAS  PubMed  Google Scholar 

  • An Z, Li C, Zhang L, Alva AK (2012) Role of polyamines and phospholipase D in maize (Zea mays L.) response to drought stress. S Afr J Bot 83:145–150

    Article  CAS  Google Scholar 

  • Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerstrom M (2006) Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47:947–959

    Article  CAS  PubMed  Google Scholar 

  • Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564

    Article  CAS  PubMed  Google Scholar 

  • Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony RG, Khan S, Costa J, Pais MS, Bogre L (2006) The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281:37536–37546

    Article  CAS  PubMed  Google Scholar 

  • Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515–522

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Burnett EC, Desikan R, Moser RC, Neill SJ (2000) ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA. J Exp Bot 51:197–205

    Article  CAS  PubMed  Google Scholar 

  • Chen YL, Huang RF, Xiao YM, Lu P, Chen J, Wang XC (2004) Extracellular calmodulin-induced stomatal closure is mediated by heterotrimeric G protein and H2O2. Plant Physiol 136:4096–4103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88

    Article  CAS  PubMed  Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212

    Article  CAS  PubMed  Google Scholar 

  • Echevarria-Machado I, Ramos-Diaz A, Brito-Argaez L, Palma GRD, Loyola-Vargas VM, Hernandez-Sotomayor SMT (2005) Polyamines modify the components of phospholipids-based signal transduction pathway in Coffea arabica L. cells. Plant Physiol Biochem 43:874–881

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Zheng S, Cui D, Wang X (1999) Subcellular distribution and tissue expression of phospholipase D alpha, D beta, and D gamma in Arabidopsis. Plant Physiol 119:1371–1378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546

    Article  CAS  PubMed  Google Scholar 

  • Farmer PK, Choi JH (1999) Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.). Bba-Protein Struct M 1434:6–17

    Article  CAS  Google Scholar 

  • Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geiger D, Maierhofer T, Al-Rasheid KA, Scherzer S, Mumm P, Liese A, Ache P, Wellmann C, Marten I, Grill E, Romeis T, Hedrich R (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4:ra32

    Article  PubMed  Google Scholar 

  • Grill E, Christmann A (2007) A plant receptor with a big family. Science 315:1676–1677

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Zheng S, Wang X (2008) Dual functions of phospholipase D alpha 1 in plant response to drought. Mol Plant 1:262–269

    Article  CAS  PubMed  Google Scholar 

  • Huang SJ, Gao L, Blanchoin L, Staiger CJ (2006) Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol Biol Cell 17:1946–1958

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311

    Article  CAS  PubMed  Google Scholar 

  • Jacob T, Ritchie S, Assmann SM, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci USA 96:12192–12197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang Y, Wu K, Lin F, Qu Y, Liu X, Zhang Q (2014) Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis. Planta 239:565–575

    Article  CAS  PubMed  Google Scholar 

  • Katagiri T, Ishiyama K, Kato T, Tabata S, Kobayashi M, Shinozaki K (2005) An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana. Plant J 43:107–117

    Article  CAS  PubMed  Google Scholar 

  • Khan BR, Zolman BK (2010) pex5 mutants that differentially disrupt PTS1 and PTS2 peroxisomal matrix protein import in Arabidopsis. Plant Physiol 154:1602–1615

    Article  CAS  PubMed Central  PubMed  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  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee S, Hirt H, Lee Y (2001) Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J 26:479–486

    Article  CAS  PubMed  Google Scholar 

  • Li G, Xue HW (2007) Arabidopsis PLD zeta 2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300–303

    Article  CAS  PubMed  Google Scholar 

  • Li G, Lin F, Xue HW (2007) Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLD beta 1 in seed germination. Cell Res 17:881–894

    Article  CAS  PubMed  Google Scholar 

  • Li W, Wang R, Li M, Li L, Wang C, Welti R, Wang X (2008) Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. J Biol Chem 283:461–468

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yue Y, Li B, Nie Y, Li W, Wu WH, Ma L (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716

    Article  CAS  PubMed  Google Scholar 

  • Loewen CJR, Gaspar ML, Jesch SA, Delon C, Ktistakis NT, Henry SA, Levine TP (2004) Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304:1644–1647

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • McPhail LC, Waite KA, Regier DS, Nixon JB, Qualliotine-Mann D, Zhang WX, Wallin R, Sergeant S (1999) A novel protein kinase target for the lipid second messenger phosphatidic acid. Bba-Mol Cell Biol L 1439:277–290

    CAS  Google Scholar 

  • Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Muller A, Giraudat J, Leung J (2007) Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J 26:3216–3226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312:264–266

    Article  CAS  PubMed  Google Scholar 

  • Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18:259–266

    Article  CAS  PubMed  Google Scholar 

  • Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327

    Article  PubMed Central  PubMed  Google Scholar 

  • Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, Yates JR, Schroeder JI (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148

    Article  CAS  PubMed  Google Scholar 

  • Park J, Gu Y, Lee Y, Yang ZB, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134:129–136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pei ZM, 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

    Article  CAS  PubMed  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  CAS  PubMed  Google Scholar 

  • Ritchie S, Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Natl Acad Sci USA 95:2697–2702

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roelfsema MR, Hedrich R, Geiger D (2012) Anion channels: master switches of stress responses. Trends Plant Sci 17:221–229

    Article  CAS  PubMed  Google Scholar 

  • Sang Y, Cui D, Wang X (2001) Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol 126:1449–1458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Marquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–588

    Article  CAS  PubMed  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    Article  CAS  PubMed  Google Scholar 

  • Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986

    Article  CAS  PubMed  Google Scholar 

  • Stark F, Pfannstiel J, Klaiber I, Raabe T (2011) Protein kinase CK2 links polyamine metabolism to MAPK signalling in Drosophila. Cell Signal 23:876–882

    Article  CAS  PubMed  Google Scholar 

  • Szostkiewicz I, Richter K, Kepka M, Demmel S, Ma Y, Korte A, Assaad FF, Christmann A, Grill E (2010) Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J 61:25–35

    Article  CAS  PubMed  Google Scholar 

  • Takemiya A, Shimazaki K (2010) Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase 1. Plant Physiol 153:1555–1562

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takemiya A, Kinoshita T, Asanuma M, Shimazaki K (2006) Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba. Proc Natl Acad Sci USA 103:13549–13554

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Testerink C, Dekker HL, Lim ZY, Johns MK, Holmes AB, de Koster CG, Ktistakis NT, Munnik T (2004) Isolation and identification of phosphatidic acid targets from plants. Plant J 39:527–536

    Article  CAS  PubMed  Google Scholar 

  • Testerink C, Larsen PB, van der Does D, van Himbergen JA, Munnik T (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J Exp Bot 58:3905–3914

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106:17588–17593

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926

    Article  CAS  Google Scholar 

  • Vahisalu T, Puzorjova I, Brosche M, Valk E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojarvi J, Loog M, Kangasjarvi J, Kollist H (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62:442–453

    Article  CAS  PubMed  Google Scholar 

  • Wang X (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139:566–573

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang C, Wang X (2001) A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiol 127:1102–1112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Noguchi K, Ono N, Inoue S, Terashima I, Kinoshita T (2014) Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth. Proc Natl Acad Sci USA 111:533–538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wimalasekera R, Villar C, Begum T, Scherer GF (2011) COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678

    Article  CAS  PubMed  Google Scholar 

  • Yakimova ET, Kapchina-Toteva VM, Laarhoven LJ, Harren FM, Woltering EJ (2006) Involvement of ethylene and lipid signalling in cadmium-induced programmed cell death in tomato suspension cells. Plant Physiol Biochem 44:581–589

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–587

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 126:1438–1448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLD delta, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase D alpha 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101:9508–9513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase d alpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W (2012) Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24:4555–4576

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao J, Zhou D, Zhang Q, Zhang W (2012) Genomic analysis of phospholipase D family and characterization of GmPLD alphas in soybean (Glycine max). J Plant Res 125:569–578

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from NSFC (91117003, 31171461) to W. Zhang and (31100194) to Q. Zhang.

Author information

Authors and Affiliations

  1. College of Life Sciences, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Yana Qu, Baocheng Zhuang, Wen Jing, Qun Zhang & Wenhua Zhang

  2. College of Life Sciences, Northwest A&F University, Yangling, 712100, People’s Republic of China

    Zhenfeng An

Authors
  1. Yana Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenfeng An
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baocheng Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wen Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhenfeng An or Wenhua Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPT 422 kb)

Fig. S1 Inhibition of CuAO activity has no effect on ABA-promoted PLD activity in Vicia faba leaves a ABA promoted PLD activity. PLD activity was measured at different times after 100 μM ABA was sprayed on leaves. b BEA had no effect on ABA-induced elevation of PLD activity. PLD activity was measured 20 min after 100 μM ABA was sprayed with or without BEA. The data are presented as the mean ± SE (n = 5). Values with different letters are significantly different at P < 0.05 based on Duncan’s multiple range test.

Fig. S2 The homology tree and gene structure of the CuAO family in Arabidopsis. a The alignment used for homology was produced with CLUSTAL W2 and manually fine-tuned using the DNAMAN software. b Gene structure of Arabidopsis CuAO. Exons and introns are represented by filled blue boxes and lines, respectively. Filled green boxes are untranslated regions.

Fig. S3 Changes of stomatal aperture in response to H2O2 and Ca2+. The epidermal peels of WT, cuaoζ and OE were incubated with 50 μM ABA, 500 μM Put, 100 μM H2O2 or 500 μM Ca2+. Stomatal apertures were measured after 2 h of treatment. The data are presented as the mean ± SE (n = 3). Values with different letters are significantly different at P < 0.05 based on Duncan’s multiple range test.

Fig. S4 Put activates PLDα1 activity in Arabidopsis. a Time course of Put-induced PLD activation in seedlings. Wide-type seedlings were treated with 200 μM Put for various times. b Western blotting of PLDα1 protein using a PLDα1-specific antibody after Put treatment, as indicated in a. c Dose dependence of Put-induced PLDα1 activation in vitro. The recombinant PLDα1 protein tagged with glutathione S-transferase (GST) at the N terminal was purified and incubated with 0.01, 0.1, 0.5 or 1 mM Put for 30 min before PLD activity assay. d Activation of PLDα1 activity by different polyamines in vitro. Put, putrescine; Spd, spermidine; Spm, spermine. The asterisks in a indicate that the mean value is significantly different from that of the control at the same time point at P < 0.05 based on Student’s t test. The data in c and d are presented as the mean ± SE (n = 3). Values with different letters are significantly different at P < 0.05 based on Duncan’s multiple range test.

Fig. S5 Quantitative reverse transcription PCR (qRT-PCR) of ABA-responsive genes. Seven-day-old seedlings of WT and cuaoζ were treated with 100 μM ABA for 2 h in liquid MS medium before extraction of total RNA. The data are presented as the mean ± SE (n = 3). Values with different letters are significantly different at P < 0.05 based on Duncan’s multiple range test.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qu, Y., An, Z., Zhuang, B. et al. Copper amine oxidase and phospholipase D act independently in abscisic acid (ABA)-induced stomatal closure in Vicia faba and Arabidopsis. J Plant Res 127, 533–544 (2014). https://doi.org/10.1007/s10265-014-0633-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-014-0633-3

Keywords

Search

Navigation