Skip to main content
SpringerLink
Log in

Phospholipase C/diacylglycerol kinase-mediated signalling is required for benzothiadiazole-induced oxidative burst and hypersensitive cell death in rice suspension-cultured cells

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary.

The involvement of phospholipase C/diacylglycerol kinase (PLC/DGK)-mediated signalling in oxidative burst and hypersensitive cell death was studied in rice suspension-cultured cells treated with benzothiadiazole (BTH) and infected by Xanthomonas oryza pv. oryza (Xoo), the causal agent of rice leaf blight disease. Treatment of rice suspension cells with BTH resulted in a significant oxidative burst, as indicated by accumulation of superoxide anion and H2O2, and hypersensitive cell death, as determined by Evans blue staining. A peak in oxidative burst was detected 3–4 h after BTH treatment and hypersensitive cell death was observed 8 h after treatment. In addition, significant oxidative burst and hypersensitive cell death were detected in BTH-treated suspension cells, but not in untreated control cells, after Xoo infection. Scavengers and antioxidants of active oxygen species, e.g., superoxide dismutase, catalase, N-acetylcysteine, and flavone, reduced significantly the BTH-induced oxidative burst and hypersensitive cell death, indicating that oxidative burst is required for BTH-induced hypersensitive cell death. Expression of the PLC/DGK pathway genes, a diacylglycerol kinase gene, OsDAGK1, and a phosphoinositide-specific phospholipase C gene, OsPI-PLC1, and a defence-related EREBP transcriptional factor gene, OsBIERF3, was activated in rice cells after BTH treatment and in the BTH-treated cells after Xoo infection. Treatment of rice cells with phosphatidic acid, a phospholipid signalling molecule, resulted in the production of oxidative burst and hypersensitive cell death. However, neomycin, a PLC inhibitor, inhibited partially but not completely the production of oxidative burst, hypersensitive cell death, and expression of OsBIERF3 and OsDAGK1 induced by BTH in rice cells. These results suggest that PLC/DGK-mediated signalling plays an important role in BTH-induced oxidative burst, hypersensitive response, and activation of defence response in rice.

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

Similar content being viewed by others

References

  • AJ Able DI Guest MW Sutherland (1998) ArticleTitleUse of a new tetrazoliumbased assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotianae Plant Physiol 117 491–499 Occurrence Handle9625702 Occurrence Handle10.1104/pp.117.2.491 Occurrence Handle1:CAS:528:DyaK1cXjvFGks7k%3D

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Song F, Goodman RM, Zheng Z (2006a) Molecular characterization of four rice ethylene-responsive element binding protein genes and their expressions in response to biotic and abiotic stresses. J Plant Physiol 163 (in press)

  • Y Cao Y Wu Z Zheng F Song (2006b) ArticleTitleOverexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco Physiol Mol Plant Pathol 67 202–211 Occurrence Handle10.1016/j.pmpp.2006.01.004

    Article  Google Scholar 

  • Z Chen DF Klessig (1991) ArticleTitleIdentification of a soluble salicylic acidbinding protein that may function in signal transduction in the plant disease-resistance response Proc Natl Acad Sci USA 88 8179–8183 Occurrence Handle11607212 Occurrence Handle10.1073/pnas.88.18.8179 Occurrence Handle1:CAS:528:DyaK3MXmtVelsrw%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Chen H Silva DF Klessig (1993) ArticleTitleActive oxygen species in the induction of plant systemic acquired resistance by salicylic acid Science 262 1883–1886 Occurrence Handle8266079 Occurrence Handle10.1126/science.8266079 Occurrence Handle1:CAS:528:DyaK2cXhtVWqu7o%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Chen J Malamy J Henning U Conrath P Sanchez-Casas H Silva J Ricigliano DK Klessig (1995) ArticleTitleInduction, modification, and transduction of the salicylic acid signal in plant defense responses Proc Natl Acad Sci USA 92 4134–4137 Occurrence Handle11607539 Occurrence Handle10.1073/pnas.92.10.4134 Occurrence Handle1:CAS:528:DyaK2MXls1alt78%3D

    Article  PubMed  CAS  Google Scholar 

  • JF Dat R Pellinen T Beeckman B Van De Cotte C Langebartels J Kangasjarvi D Inze F Van Breusegem (2003) ArticleTitleChanges in hydrogen peroxide homeostasis trigger an active cell death process in tobacco Plant J 33 621–632 Occurrence Handle12609037 Occurrence Handle10.1046/j.1365-313X.2003.01655.x Occurrence Handle1:CAS:528:DC%2BD3sXislWiurw%3D

    Article  PubMed  CAS  Google Scholar 

  • CF de Jong AM Laxalt BO Bargmann PJ de Wit MH Joosten T Munnik (2004) ArticleTitlePhosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction Plant J 39 1–12 Occurrence Handle15200638 Occurrence Handle10.1111/j.1365-313X.2004.02110.x Occurrence Handle1:CAS:528:DC%2BD2cXms1yktbo%3D

    Article  PubMed  CAS  Google Scholar 

  • M den Hartog A Musgrave T Munnik (2001) ArticleTitleNod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair formation Plant J 25 55–65 Occurrence Handle11169182 Occurrence Handle10.1046/j.1365-313x.2001.00931.x Occurrence Handle1:CAS:528:DC%2BD3MXhsVWrtrc%3D

    Article  PubMed  CAS  Google Scholar 

  • M den Hartog N Verhoef T Munnik (2003) ArticleTitleNod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells Plant Physiol 132 311–317 Occurrence Handle12746536 Occurrence Handle10.1104/pp.102.017954 Occurrence Handle1:CAS:528:DC%2BD3sXktVGgsb0%3D

    Article  PubMed  CAS  Google Scholar 

  • J Durner DF Klessig (1995) ArticleTitleInhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses Proc Natl Acad Sci USA 92 11312–11316 Occurrence Handle7479986 Occurrence Handle10.1073/pnas.92.24.11312 Occurrence Handle1:CAS:528:DyaK2MXps1altb4%3D

    Article  PubMed  CAS  Google Scholar 

  • J Foreman V Demidchik JH Bothwell P Mylona H Miedema MA Torres P Linstead S Costa C Brownlee JD Jones JM Davies L Dolan (2003) ArticleTitleReactive oxygen species produced by NADPH oxidase regulate plant cell growth Nature 422 442–446 Occurrence Handle12660786 Occurrence Handle10.1038/nature01485 Occurrence Handle1:CAS:528:DC%2BD3sXitlGgtLg%3D

    Article  PubMed  CAS  Google Scholar 

  • X Ge F Song Z Zheng (1999) ArticleTitleSystemic acquired resistance to Magnaporthe grisea in rice induced by BTH Acta Agric Zhejiangensis 11 311–314

    Google Scholar 

  • XC Ge FM Song Z Zheng (2000) ArticleTitleActive oxygen species in rice seedlings infected with Magnaporthe grisea is involved in the blast resistance Acta Phytophysiol Sin 26 227–231 Occurrence Handle1:CAS:528:DC%2BD3cXms1arsrc%3D

    CAS  Google Scholar 

  • J Gorlach S Volrath G Knauf-Beiter G Hengy U Beckhove K-H Kogel M Oostendorp T Staub E Ward H Kessmann J Ryals (1996) ArticleTitleBenzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat Plant Cell 8 629–643 Occurrence Handle8624439 Occurrence Handle10.1105/tpc.8.4.629 Occurrence Handle1:STN:280:BymB3cnotFA%3D

    Article  PubMed  CAS  Google Scholar 

  • JJ Grant GJ Loake (2000) ArticleTitleRole of reactive oxygen intermediates and cognate redox signaling in disease resistance Plant Physiol 124 21–29 Occurrence Handle10982418 Occurrence Handle10.1104/pp.124.1.21 Occurrence Handle1:CAS:528:DC%2BD3cXmvVGhsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • Z He ZY Wang J Li Q Zhu C Lamb P Ronald J Chory (2000) ArticleTitlePerception of brassinosteroids by the extracellular domain of the receptor kinase BRI1 Science 288 2360–2363 Occurrence Handle10875920 Occurrence Handle10.1126/science.288.5475.2360 Occurrence Handle1:CAS:528:DC%2BD3cXkslWisrk%3D

    Article  PubMed  CAS  Google Scholar 

  • T Jabs RA Dietrich JL Dangl (1996) ArticleTitleInitiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide Science 273 1853–1856 Occurrence Handle8791589 Occurrence Handle10.1126/science.273.5283.1853 Occurrence Handle1:CAS:528:DyaK28XlvFCrsLk%3D

    Article  PubMed  CAS  Google Scholar 

  • VA Katz OU Thulke U Conrath (1998) ArticleTitleA benzothiadiazole primes parsley cells for augmented elicitation of defense responses Plant Physiol 117 1333–1339 Occurrence Handle9701589 Occurrence Handle10.1104/pp.117.4.1333 Occurrence Handle1:CAS:528:DyaK1cXlsFaqtLc%3D

    Article  PubMed  CAS  Google Scholar 

  • H Kauss W Jeblick (1995) ArticleTitlePretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2 Plant Physiol 108 1171–1178 Occurrence Handle12228535 Occurrence Handle1:CAS:528:DyaK2MXmvFGmur0%3D

    PubMed  CAS  Google Scholar 

  • A Kohler S Schwindling U Conrath (2002) ArticleTitleBenzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis Plant Physiol 128 1046–1056 Occurrence Handle11891259 Occurrence Handle10.1104/pp.010744 Occurrence Handle1:CAS:528:DC%2BD38Xit1GqtLo%3D

    Article  PubMed  CAS  Google Scholar 

  • JM Kwak IC Mori ZM Pei N Leonhardt MA Torres JL Dangl RE Bloom S Bodde JD Jones JI Schroeder (2003) ArticleTitleNADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis EMBO J 22 2623–2633 Occurrence Handle12773379 Occurrence Handle10.1093/emboj/cdg277 Occurrence Handle1:CAS:528:DC%2BD3sXkt1WrtLY%3D

    Article  PubMed  CAS  Google Scholar 

  • C Lamb RA Dixon (1997) ArticleTitleThe oxidative burst in plant disease resistance Annu Rev Plant Physiol Plant Mol Biol 48 251–275 Occurrence Handle15012264 Occurrence Handle10.1146/annurev.arplant.48.1.251 Occurrence Handle1:CAS:528:DyaK2sXjs1entr8%3D

    Article  PubMed  CAS  Google Scholar 

  • AM Laxalt T Munnik (2002) ArticleTitlePhospholipid signalling in plant defence Curr Opin Plant Biol 5 332–338 Occurrence Handle12179967 Occurrence Handle10.1016/S1369-5266(02)00268-6 Occurrence Handle1:CAS:528:DC%2BD38Xls1ejtLg%3D

    Article  PubMed  CAS  Google Scholar 

  • L Legendre YG Yueh R Crain N Haddock PF Heinstein PS Low (1993) ArticleTitlePhospholipase C activation during elicitation of the oxidative burst in cultured plant cells J Biol Chem 268 24559–24563 Occurrence Handle8227014 Occurrence Handle1:CAS:528:DyaK3sXmt1Wktrc%3D

    PubMed  CAS  Google Scholar 

  • A Levine R Tenhaken R Dixon C Lamb (1994) ArticleTitleH2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response Cell 79 583–593 Occurrence Handle7954825 Occurrence Handle10.1016/0092-8674(94)90544-4 Occurrence Handle1:CAS:528:DyaK2MXit1Glu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • LC McPhail KA Waite DS Regier JB Nixon D Qualliotine-Mann WX Zhang R Wallin S Sergeant (1999) ArticleTitleA novel protein kinase target for the lipid second messenger phosphatidic acid Biochim Biophys Acta 1439 277–290 Occurrence Handle10425401 Occurrence Handle1:CAS:528:DyaK1MXkvFKhs7s%3D

    PubMed  CAS  Google Scholar 

  • HJ Meijer T Munnik (2003) ArticleTitlePhospholipid-based signaling in plants Annu Rev Plant Physiol Plant Mol Biol 54 265–306 Occurrence Handle1:CAS:528:DC%2BD3sXntFSgu7g%3D

    CAS  Google Scholar 

  • J Morel J Fromentin JP Blein F Simon-Plas T Elmayan (2004) ArticleTitleRac regulation of NtrbohD, the oxidase responsible for the oxidative burst in elicited tobacco cell Plant J 37 282–293 Occurrence Handle14690511 Occurrence Handle1:CAS:528:DC%2BD2cXhsVGlur0%3D

    PubMed  CAS  Google Scholar 

  • T Munnik (2001) ArticleTitlePhosphatidic acid: an emerging plant lipid second messenger Trends Plant Sci 6 227–233 Occurrence Handle11335176 Occurrence Handle10.1016/S1360-1385(01)01918-5 Occurrence Handle1:CAS:528:DC%2BD3MXlsFKmtbs%3D

    Article  PubMed  CAS  Google Scholar 

  • T Munnik RF Irvine A Musgrave (1998) ArticleTitlePhospholipid signalling in plants Biochim Biophys Acta 1389 222–272 Occurrence Handle9512651 Occurrence Handle1:CAS:528:DyaK1cXhsFaqu7o%3D

    PubMed  CAS  Google Scholar 

  • J Park Y Gu Y Lee Z Yang Y Lee (2004) ArticleTitlePhosphatidic 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 Occurrence Handle14730067 Occurrence Handle10.1104/pp.103.031393 Occurrence Handle1:CAS:528:DC%2BD2cXhtVagur8%3D

    Article  PubMed  CAS  Google Scholar 

  • DS Regier DG Greene S Sergeant AJ Jesaitis LC McPhail (2000) ArticleTitlePhosphorylation of p22phox is mediated by phospholipase D-dependent and -independent mechanisms. Correlation of NADPH oxidase activity and p22phox phosphorylation J Biol Chem 275 28406–28412 Occurrence Handle10893420 Occurrence Handle10.1074/jbc.M004703200 Occurrence Handle1:CAS:528:DC%2BD3cXms1Cruro%3D

    Article  PubMed  CAS  Google Scholar 

  • Y Sang D Cui X Wang (2001) ArticleTitlePhospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis Plant Physiol 126 1449–1458 Occurrence Handle11500544 Occurrence Handle10.1104/pp.126.4.1449 Occurrence Handle1:CAS:528:DC%2BD3MXlvFOjurs%3D

    Article  PubMed  CAS  Google Scholar 

  • F Song RM Goodman (2002) ArticleTitleMolecular cloning and characterization of a rice phosphoinositide-specific phospholipase C gene, OsPI-PLC1 that is activated in systemic acquired resistance Physiol Mol Plant Pathol 61 31–40 Occurrence Handle1:CAS:528:DC%2BD38XnvFWjsrY%3D

    CAS  Google Scholar 

  • F Song X Ge Z Zheng Y Xie (2001) ArticleTitleBenzothiadiazole induces systemic acquired resistance in rice against bacterial leaf blight Chin J Rice Sci 15 323–326

    Google Scholar 

  • C Testerink T Munnik (2005) ArticleTitlePhosphatidic acid: a multifunctional stress signaling lipid in plants Trends Plant Sci 10 368–375 Occurrence Handle16023886 Occurrence Handle10.1016/j.tplants.2005.06.002 Occurrence Handle1:CAS:528:DC%2BD2MXmvVCmsrs%3D

    Article  PubMed  CAS  Google Scholar 

  • MA Torres JL Dangl JD Jones (2002) ArticleTitleArabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response Proc Natl Acad Sci USA 99 517–522 Occurrence Handle11756663 Occurrence Handle10.1073/pnas.012452499 Occurrence Handle1:CAS:528:DC%2BD38Xlt1CqsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • MA Torres JD Jones JL Dangl (2005) ArticleTitlePathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana Nat Genet 37 1130–1134 Occurrence Handle16170317 Occurrence Handle10.1038/ng1639 Occurrence Handle1:CAS:528:DC%2BD2MXhtVCntL%2FN

    Article  PubMed  CAS  Google Scholar 

  • AH Van der Luit T Piatti A Van Doorn A Musgrave G Felix T Boller T Munnik (2000) ArticleTitleElicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate Plant Physiol 123 1507–1515 Occurrence Handle10938366 Occurrence Handle10.1104/pp.123.4.1507 Occurrence Handle1:CAS:528:DC%2BD3cXmtVegsr8%3D

    Article  PubMed  CAS  Google Scholar 

  • D Wendehenne J Durner F Daniel (1998) ArticleTitleBenzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidase Phytochemistry 47 651–657 Occurrence Handle10.1016/S0031-9422(97)00604-3 Occurrence Handle1:CAS:528:DyaK1cXmtFCksg%3D%3D

    Article  CAS  Google Scholar 

  • P Wojtaszek (1997) ArticleTitleOxidative burst: an early plant response to pathogen infection Biochem J 322 681–692 Occurrence Handle9148737 Occurrence Handle1:CAS:528:DyaK2sXit1Ojsrs%3D

    PubMed  CAS  Google Scholar 

  • T Yamaguchi E Eiichi Minami N Shibuya (2003) ArticleTitleActivation of phospholipases by N-acetylchitooligosaccharide elicitor in suspension-cultured rice cells mediates reactive oxygen generation Physiol Plant 118 361–370 Occurrence Handle10.1034/j.1399-3054.2003.00131.x Occurrence Handle1:CAS:528:DC%2BD3sXlsVSisL4%3D

    Article  CAS  Google Scholar 

  • T Yamaguchi S Tanabe E Minami N Shibuya (2004) ArticleTitleActivation of phospholipase D induced by hydrogen peroxide in suspension-cultured rice cells Plant Cell Physiol 45 1261–1270 Occurrence Handle15509849 Occurrence Handle10.1093/pcp/pch150 Occurrence Handle1:CAS:528:DC%2BD2cXptVKltb4%3D

    Article  PubMed  CAS  Google Scholar 

  • T Yamaguchi E Minami J Ueki N Shibuya (2005) ArticleTitleElicitor-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 Occurrence Handle15695430 Occurrence Handle10.1093/pcp/pci065 Occurrence Handle1:CAS:528:DC%2BD2MXjslGrtL0%3D

    Article  PubMed  CAS  Google Scholar 

  • H Yoshioka N Numata K Nakajima S Katou K Kawakita O Rowland JD Jones N Doke (2003) ArticleTitle Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans Plant Cell 15 706–718 Occurrence Handle12615943 Occurrence Handle10.1105/tpc.008680 Occurrence Handle1:CAS:528:DC%2BD3sXisVektLc%3D

    Article  PubMed  CAS  Google Scholar 

  • SA Young X Wang JE Leach (1996) ArticleTitleChanges in the plasma membrane distribution of rice phospholipase D during resistant interactions with Xanthomonas oryzae pv. oryzae Plant Cell 8 1079–1090 Occurrence Handle12239412 Occurrence Handle10.1105/tpc.8.6.1079 Occurrence Handle1:CAS:528:DyaK28XjvFSqsLc%3D

    Article  PubMed  CAS  Google Scholar 

  • W Zhang X Ge F Song Z Zheng (2003) ArticleTitleSystemic acquired resistance of rice against sheath blight disease induced by benzothiadiazole Acta Phytophylacica Sin 30 171–176 Occurrence Handle1:CAS:528:DC%2BD2cXhsFSmtbg%3D

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang

    Jie Chen, Weidong Zhang, Fengming Song & Zhong Zheng

  2. Department of Plant Protection, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang

    Jie Chen, Weidong Zhang, Fengming Song & Zhong Zheng

  3. State Key Laboratory for Rice Biology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang

    Fengming Song

Authors
  1. Jie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weidong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fengming Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhong Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengming Song.

Additional information

Correspondence and reprints: Department of Plant Protection, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310029, People’s Republic of China.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, J., Zhang, W., Song, F. et al. Phospholipase C/diacylglycerol kinase-mediated signalling is required for benzothiadiazole-induced oxidative burst and hypersensitive cell death in rice suspension-cultured cells. Protoplasma 230, 13–21 (2007). https://doi.org/10.1007/s00709-006-0195-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-006-0195-x

Search

Navigation