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Endogenous hydrogen peroxide is a key factor in the yeast extract-induced activation of biphenyl biosynthesis in cell cultures of Sorbus aucuparia

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Abstract

Biphenyls are unique phytoalexins produced by plants belonging to Pyrinae, a subtribe of the economically important Rosaceae family. The formation of aucuparin, a well-known biphenyl, is induced by yeast extract (YE) in cell cultures of Sorbus aucuparia. However, the molecular mechanism underlying YE-induced activation of biphenyl biosynthesis remains unknown. Here we demonstrate that the addition of YE to the cell cultures results in a burst of reactive oxygen species (ROS; H2O2 and O2 −), followed by transcriptional activation of the biphenyl synthase 1 gene (BIS1) encoding the key enzyme of the biphenyl biosynthetic pathway and aucuparin accumulation. Pretreatment of the cell cultures with ROS scavenger dihydrolipoic acid and NADPH oxidase-specific inhibitor diphenylene iodonium abolished all of the above YE-induced biological events. However, when the cell cultures was pretreated with superoxide dismutase specific inhibitor N,N-diethyldithiocarbamic acid, although O2 − continued to be generated, the H2O2 accumulation, BIS1 expression and aucuparin production were blocked. Interestingly, exogenous supply of H2O2 in the range of 0.05–10 mM failed to induce aucuparin accumulation. These results indicate that endogenous generation of H2O2 rather than that of O2 − is a key factor in YE-induced accumulation of biphenyl phytoalexins in cell cultures of S. aucuparia.

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Abbreviations

BIS:

Biphenyl synthase

DHLA:

Dihydrolipoic acid

DIECA:

Diethyldithiocarbamic acid

DPI:

Diphenylene iodonium

NBT:

Nitroblue tetrazolium

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

YE:

Yeast extract

References

  • Auh CK, Murphy TM (1995) Plasma-membrane redox enzyme is involved in the synthesis of O2 − and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol 107:1241–1247

    PubMed  CAS  Google Scholar 

  • Beaucham CO, Fridovic I (1973) Isoenzymes of superoxide dismutase from wheat-germ. Biochim Biophys Acta 317:50–64

    Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide-dismutase activity—some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  PubMed  CAS  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  PubMed  CAS  Google Scholar 

  • Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 2:287–294

    Article  PubMed  CAS  Google Scholar 

  • Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence—a broad perspective. Physiol Mol Plant Pathol 51:347–366

    Article  CAS  Google Scholar 

  • 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. J Exp Bot 53:1367–1376

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bruinsma M, van Loon JJ, Dicke M (2010) Increasing insight into induced plant defense mechanisms using elicitors and inhibitors. Plant Signal Behav 5:271–274

    Article  PubMed  CAS  Google Scholar 

  • Chandra S, Low PS (1995) Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proc Natl Acad Sci USA 92:4120–4123

    Article  PubMed  CAS  Google Scholar 

  • Chung KM, Igari K, Uchida N, Tasaka M (2008) New perspectives on plant defense responses through modulation of developmental pathways. Mol Cells 26:107–112

    PubMed  CAS  Google Scholar 

  • Davies DR, Bindschedler LV, Strickland TS, Bolwell GP (2006) Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: implications for basal resistance. J Exp Bot 57:1817–1827

    Article  PubMed  CAS  Google Scholar 

  • Degousee N, Triantaphylides C, Montillet JL (1994) Involvement of oxidative processes in the signaling mechanisms leading to the activation of glyceollin synthesis in soybean (Glycine-max). Plant Physiol 104:945–952

    PubMed  CAS  Google Scholar 

  • Desikan R, Hancock JT, Coffey MJ, Neill SJ (1996) Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett 382:213–217

    Article  PubMed  CAS  Google Scholar 

  • Francisca S, Julio L, Luis A (1982) Characterization of a manganese superoxide dismutase from the higher plant Pisum sativum. Plant Physiol 70:1321–1326

    Article  Google Scholar 

  • Guo ZJ, Lamb C, Dixon RA (1998) Potentiation of the oxidative burst and isoflavonoid phytoalexin accumulation by serine protease inhibitors. Plant Physiol 118:1487–1494

    Article  PubMed  CAS  Google Scholar 

  • Huettner C, Beuerle T, Scharnhop H, Ernst L, Beerhues L (2010) Differential effect of elicitors on biphenyl and dibenzofuran formation in Sorbus aucuparia cell cultures. J Agric Food Chem 58:11977–11984

    Article  Google Scholar 

  • Jabs T, Tschope M, Colling C, Hahlbrock K, Scheel D (1997) Elicitor-stimulated ion fluxes and O2 − from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 94:4800–4805

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Kokubun T, Harborne JB (1995) Phytoalexin induction in the sapwood of plants of the maloideae (Rosaceae)—biphenyls or dibenzofurans. Phytochemistry 40:1649–1654

    Article  CAS  Google Scholar 

  • Kokubun T, Harborne JB, Eagles J, Waterman PG (1995) Antifungal biphenyl compounds are the phytoalexins of the sapwood of Sorbus aucuparia. Phytochemistry 40:57–59

    Article  CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Beuerle T, Klundt T, Beerhues L (2004) Biphenyl synthase from yeast-extract-treated cell cultures of Sorbus aucuparia. Planta 218:492–496

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Raeth T, Beuerle T, Beerhues L (2007) Biphenyl synthase, a novel type III polyketide synthase. Planta 225:1495–1503

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Raeth T, Beuerle T, Beerhues L (2010) A novel 4-hydroxycoumarin biosynthetic pathway. Plant Mol Biol 72:17–25

    Article  PubMed  CAS  Google Scholar 

  • Moller IM, Sweetlove LJ (2010) ROS signalling—specificity is required. Trends Plant Sci 15:370–374

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic-acid and hydrogen-peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141:346–350

    Article  PubMed  CAS  Google Scholar 

  • Sarath G, Hou GC, Baird LM, Mitchell RB (2007) Reactive oxygen species, ABA and nitric oxide interactions on the germination of warm-season C4-grasses. Planta 226:697–708

    Article  PubMed  CAS  Google Scholar 

  • Van Gestelen P, Asard H, Horemans N, Caubergs RJ (1998) Superoxide-producing NAD(P)H oxidases in plasma membrane vesicles from elicitor responsive bean plants. Physiol Plant 104:653–660

    Article  Google Scholar 

  • Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol 154:444–448

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Suzuki K, Shinshi H (1999) Elicitor-responsive, ethylene-independent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. Plant J 20:571–579

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Zou T, Lu YH, Wang JW (2010) Stimulation of artemisinin biosynthesis in Artemisia annua hairy roots by oligogalacturonides. Afr J Biotechnol 9:3437–3442

    CAS  Google Scholar 

  • Zhao J, Sakai K (2003) Multiple signalling pathways mediate fungal elicitor-induced beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 54:647–656

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Hu Q, Guo YQ, Zhu WH (2001) Elicitor-induced indole alkaloid biosynthesis in Catharanthus roseus cell cultures is related to Ca2+ influx and the oxidative burst. Plant Sci 161:423–431

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work was financially supported by the National Sciences Foundation of China (30870217).

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Authors and Affiliations

  1. Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, The Chinese Academy of Sciences, Nanxincun 20, Haidian District, Beijing, 100093, China

    Xiaofang Qiu, Caiyan Lei, Lili Huang, Xing Li, Zhigao Du, Hechun Ye & Benye Liu

  2. Institute of Pharmaceutical Biology, Technische Universität Braunschweig, Mendelssohnstraße 1, 38106, Brunswick, Germany

    Ludger Beerhues & Benye Liu

  3. Graduate University of The Chinese Academy of Sciences, 19A Yuquanlu, Beijing, 100049, China

    Xiaofang Qiu, Caiyan Lei, Xing Li, He Hao & Hong Wang

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  1. Xiaofang Qiu
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  2. Caiyan Lei
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  3. Lili Huang
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  4. Xing Li
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  5. He Hao
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  6. Zhigao Du
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  7. Hong Wang
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  8. Hechun Ye
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  9. Ludger Beerhues
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  10. Benye Liu
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Correspondence to Hong Wang or Benye Liu.

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Qiu, X., Lei, C., Huang, L. et al. Endogenous hydrogen peroxide is a key factor in the yeast extract-induced activation of biphenyl biosynthesis in cell cultures of Sorbus aucuparia . Planta 235, 217–223 (2012). https://doi.org/10.1007/s00425-011-1545-2

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  • DOI: https://doi.org/10.1007/s00425-011-1545-2

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