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Bisorbicillinoids Produced by the Fungus Trichoderma citrinoviride Affect Feeding Preference of the Aphid Schizaphis graminum

Journal of Chemical Ecology volume 35, pages 533–541 (2009)Cite this article

Abstract

We report the effects of some bisorbicillinoids isolated from biomass of the fungus Trichoderma citrinoviride on settling and feeding preference of the aphid Schizaphis graminum. Purification of the fungal metabolites was carried out by a combination of column chromatography and thin-layer chromatography using direct and reverse phases. Chemical identification was performed by spectroscopic methods including nuclear magnetic resonance and mass spectrometry. The identified bisorbicillinoids appeared to be bislongiquinolide, its 16,17-dihydro derivative, trichodimerol, and dihydrotrichodimerol. A feeding preference test with alate morphs of S. graminum was used to identify the active fractions. Among the four bisorbicillinoids, dihydrotrichodimerol and bislongiquinolide influenced aphid feeding preference, restraining specimens from settling on leaves treated with metabolites. Taste neurons sensitive to these compounds, particularly to bislongiquinolide, were located on tarsi of the S. graminum alate morphs.

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References

  • Abe N., Murata T., Hirota A. Novel DPPH radical scavengers, bisorbicillinol and demethyltrichodimerol, from a fungus. Biosc. Biotechnol. Biochem. 1998;62:661–666.

    Article  CAS  Google Scholar 

  • Abe N., Murata T., Yamamoto K., Hirota A. Bisorbibetanone, a novel oxidized sorbicillin dimmer, with 1, 1-diphenyl-2-picrylhydrazyl radical scavenging activity from a fungus. Tetrahedron Lett. 1999;40:5203–5206.

    Article  CAS  Google Scholar 

  • Abe N., Arakawa T., Yamamoto K., Hirota A. Biosynthesis of bisorbicillinoid in Trichoderma sp. USF-2690; evidence for the biosynthetic pathway, via sorbicillinol, of sorbicillin, bisorbicillinol, bisorbibutenolide, and bisorbicillinolide. Biosc. Biotechnol. Biochem. 2002;66:2090–2099.

    Article  CAS  Google Scholar 

  • Ambrosi P., Arnone A., Bravo P., Bruchè L., De Cristofaro A., Francardi V., et al. Stereoselective synthesis of trifluoro- and monofluoro-analogues of frontalin and evaluation of their biological activity. J. Org. Chem. 2001;66:8336–8343.

    PubMed  Article  CAS  Google Scholar 

  • Amiri B., Ibrahim L., Butt T. Antifeedant properties of destruxins and their potential use with the entomogenous fungus Metarhizium anisopliae for improved control of crucifer pest. Biocontrol Sci. Techn. 1999;9:487–498.

    Article  Google Scholar 

  • Andrade R., Ayer W.A., Mebe P.P. The metabolites of Trichoderma longibrachiatum. Part 1. Isolation of the metabolites and the structure of trichodimerol. Can. J. Chem. 1997;70:2526–2535.

    Article  Google Scholar 

  • Berger S., Braun S. 200 and More NMR Experiments. Weinheim: Wiley-VCH; 2004.

    Google Scholar 

  • Bissett J. A revision of the genus Trichoderma. I. Section Longibrachiatum sect. nov. Canad. J. Bot. 1984;62:924–931.

    Article  Google Scholar 

  • Bissett J. A revision of the genus Trichoderma. IV. Additional notes on section Longibrachiatum. Canad. J. Bot. 1991;69:2418–2420.

    Article  Google Scholar 

  • Crnjar R.M., Prokopy R.J. Morphological and electrophysiological mapping of tarsal chemoreceptors of oviposition deterring pheromone in Rhagoletis pomonella flies. J. Insect Physiol. 1982;28:393–400.

    Article  Google Scholar 

  • De Cristofaro A., Ioriatti C., Pasqualini E., Anfora G., Germinara G.S., Villa M., et al. Electrophysiological responses of Cydia pomonella to codlemone and pear ester ethyl (E,Z)-2,4-decadienoate: peripheral interactions in their perception and evidences for cells responding to both compounds. Bull. Insectol. 2004;57:137–144.

    Google Scholar 

  • Den Otter C.J., Van Der Starre H. Responses of tarsal hairs of the bluebottle, Calliphora erythrocephala Meig., to sugar and water. J. Insect Physiol. 1967;13:1177–1188.

    Article  Google Scholar 

  • Ekesi S., Egwurube E.A., Akpa A.D., Onu I. Laboratory evaluation of the entomopathogenic fungus, Metarhizium anisopliae for the control of the groundnut bruchid, Caryedon serratus on groundnut. J. Stored Prod. Res. 2001;37:313–321.

    PubMed  Article  Google Scholar 

  • Evidente A., Ricciardiello G., Andolfi A., Sabatini M.A., Ganassi S., Altomare C., et al. Citrantifidiene and citrantifidiol: bioactive metabolites produced by Trichoderma citrinoviride with potential antifeedant activity toward aphids. J. Agric. Food Chem. 2008;56:3569–3573.

    PubMed  Article  CAS  Google Scholar 

  • Ganassi S., De Cristofaro A., Grazioso P., Altomare C., Logrieco A., Sabatini M.A. Detection of fungal metabolites of various Trichoderma species by the aphid Schizaphis graminum. Entomol. Exp. Appl. 2007;122:77–86.

    Article  Google Scholar 

  • Gao Q., Leet J.E., Thomas S.T., Matson J.A. Crystal structure of trichodimerol. J. Nat. Prod. 1995;58:1817–1821.

    Article  CAS  Google Scholar 

  • Hodgson E.S., Lettvin J.Y., Roeder K.D. Physiology of a primary chemoreceptor unit. Science. 1955;122:417–418.

    PubMed  Article  CAS  Google Scholar 

  • Kaissling K.E. Single unit and electroantennogram recordings in insect olfactory organs, pp. 361–377. In: Spielman AI, Brand JG, editors. Experimental Cell Biology of Taste and Olfaction: Current Techniques and Protocols. Boca Raton, New York: CRC Press; 1995.

    Google Scholar 

  • Kuhls K., Lieckfeldt E., Borner T., Gueho E. Molecular reidentification of human pathogenic Trichoderma isolates as Trichoderma longibrachiatum and Trichoderma citrinoviride. Med. Mycol. 1999;37:25–33.

    PubMed  CAS  Google Scholar 

  • Lee D., Lee J.H., Cia X.F., Shin J.C., Lee K., Hong Y.S., et al. Fungal metabolites, sorbicillinoid polyketides and their effects on the activation of peroxisome proliferator-activated receptor γ. J. Antibiot. 2005;58:615–620.

    PubMed  Article  CAS  Google Scholar 

  • Liu W., Gu Q., Zhu W., Cui C., Fan G. Dihydrotrichodimerol, and tetrahydrotrichodimerol, two new bisorbicillinoids, from a marine-derived Penicillium terrestre. J. Antibiot. 2005;58:621–624.

    PubMed  Article  CAS  Google Scholar 

  • Maher N., Thiery D. Distribution of chemo- and mechanoreceptors on the tarsi and ovipositor of female European grapevine moth, Lobesia botrana. Entomol. Exp. Appl. 2004;110:135–143.

    Article  Google Scholar 

  • Marion-poll F., Van der pers J.N.C. Un-filtered recordings from insect taste sensilla. Entomol. Exp. Appl. 1996;80:113–118.

    Article  Google Scholar 

  • Maskey R.P., Grün-wollny I., Laatsgh H. Sorbicillin analogues and related dimeric compounds from Penicillium notatum. J. Nat. Prod. 2005;68:865–870.

    PubMed  Article  CAS  Google Scholar 

  • Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 1983;65:55–63.

    PubMed  Article  CAS  Google Scholar 

  • Mulè G., D'Ambrosio A., Logrieco A., Bottalico A. Toxicity of mycotoxins of Fusarium sambucinum for feeding in Galleria mellonella. Entomol. Exp. Appl. 1992;62:17–22.

    Article  Google Scholar 

  • Nicolaou K.C., Jautelat R., Vassilikogiannakis G., Baran P.S., Simonsen K.B. Studies towards trichodimerol: novel cascade reactions and polycyclic frameworks. Chem. Eur. J. 1999;5:3651–3665.

    Article  CAS  Google Scholar 

  • Nicolaou K.C., Vassilikogiannakis G., Simonsen K.B., Baran P.S., Zhong Y.L., Vidali V.P., et al. Biomimetic total synthesis of bisorbicillinol, bisorbutenolide, trichodimerol, and designed analogues of bisorbicillinoids. J. Am. Chem. Soc. 2000;122:3071–3079.

    Article  CAS  Google Scholar 

  • Pickett J.A., Dawson G.W., Griffiths D.C., Hassanali A., Merritt L.A., Mudd A., et al. Development of plant-derived antifeedants for crop protection, pp. 125–128. In: Greenhalgh R, Roberts TR, editors. Pesticide Science and biotechnology. Oxford: Blackwell Scientific; 1987.

    Google Scholar 

  • Pitsinos E.N., Vidali P.V., Couladouros E.A. Synthetic studies towards trichodimerol and related polyketide. Arch. Org. Chem. 2008;13:105–110.

    Google Scholar 

  • Sabatini M.A., Innocenti G. Functional relationships between Collembola and plant pathogenic fungi of agricultural soils. Pedobiologia. 2000;44:467–475.

    Article  Google Scholar 

  • Samuels G.J., Petrini O., Kuhls K., Lieckfeldt E., Kubicek C.P. The Hypocrea schweinitzii complex and Trichoderma sect. Longibrachiatum. Stud. Mycol. 1998;41:1–54.

    Google Scholar 

  • Saxena S., Pandey A.K. Microbial metabolites as eco-friendly agrochemicals for the next millennium. Appl. Microbiol. Biotechnol. 2001;55:395–403.

    PubMed  Article  CAS  Google Scholar 

  • Shirota O., Pathak V., Hossain C.F., Sekita S., Takatori K., Satake M. Structural elucidation of trichotetronines: polyketides possessing a bicyclo[2.2.2]octane skeleton with tetronic acid moiety isolated from Trichoderma sp. J. Chem. Soc. Perkin Trans. 1997;I:2961–2964.

    Article  Google Scholar 

  • Solinas M., Rebora M., De cristofaro A., Rotundo G., Girolami V., Mori N., et al. Functional morphology of Bactrocera oleae (Diptera: Tephritidae) tarsal chemosensilla involved in interactions with host-plant. Entomologica. 2001;35:103–123.

    Google Scholar 

  • Sperry S., Samuels G.J., Crews P. Vertinol polyketides from the saltwater culture of the fungus Trichoderma longibrachiatum separated from a Haliclona marine sponge. J. Org. Chem. 1998;63:10011–10014.

    Article  CAS  Google Scholar 

  • Tanaka Y., Ōmura S. Agroactive compounds of microbial-origin Ann. Rev. Microbiol. 1993;47:57–87.

    Article  CAS  Google Scholar 

  • Trifonov L.S., Bieri J.H., Prewo R., Dreiding A.S., Hoesch L., Rast D.M. Isolation and structure elucidation of three metabolites from Verticillium intertextum: sorbicillin, dihydrosorbicillin and bisvertinoquinol. Tetrahedron. 1983;39:4243–4256.

    Article  CAS  Google Scholar 

  • Trifonov L.S., Hilpert H., Floersheim P., Dreiding A.S., Rast D.M., Skrivanova R., et al. Bisvertinols: a new group of dimeric vertinoids from Verticillium intertextum. Tetrahedron. 1986;42:3157–3179.

    Article  CAS  Google Scholar 

  • Wright V.F., Vesonder R.F., Ciegler A. Mycotoxins and other fungal metabolites as insecticides, pp. 559–583. In: Kurstak E., editor. Microbial and Viral Pesticides. New York & Basel: Dekker; 1982.

    Google Scholar 

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Acknowledgment

The NMR spectra were recorded at the NMR Service of the Istituto di Chimica Biomolecolare del CNR, Pozzuoli, Italy. Dr. G. Ricciardiello and Mrs D. Melck are gratefully acknowledged for technical assistance and Mrs. M. Zampa for recording MS spectra. The authors also acknowledge the assistance of Dr. Pasqualina Grazioso for statistical analysis. The work was supported by a grant from the Italian Ministry of University and Research (MIUR). Contribution DISSPAPA n. 162.

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Affiliations

  1. Dipartimento di Scienze del Suolo, della Pianta, dell’Ambiente e delle Produzioni Animali, Università di Napoli Federico II, Via Università 100, 80055, Portici, Italy

    Antonio Evidente, Anna Andolfi & Alessio Cimmino

  2. Dipartimento di Biologia Animale, Università di Modena e Reggio Emilia, Via Campi 213/D, 41100, Modena, Italy

    Sonia Ganassi & Maria Agnese Sabatini

  3. Istituto di Scienze delle Produzioni Alimentari del CNR, Via Amendola, 122/O, 70126, Bari, Italy

    Claudio Altomare & Mara Favilla

  4. Dipartimento di Scienze Animali, Vegetali e dell’Ambiente, Università del Molise, Via De Sanctis, 86100, Campobasso, Italy

    Antonio De Cristofaro & Silvia Vitagliano

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  1. Antonio Evidente
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  2. Anna Andolfi
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  9. Maria Agnese Sabatini
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Correspondence to Antonio Evidente.

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Evidente, A., Andolfi, A., Cimmino, A. et al. Bisorbicillinoids Produced by the Fungus Trichoderma citrinoviride Affect Feeding Preference of the Aphid Schizaphis graminum . J Chem Ecol 35, 533–541 (2009). https://doi.org/10.1007/s10886-009-9632-6

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  • DOI: https://doi.org/10.1007/s10886-009-9632-6

Keywords

  • Aphids
  • Schizaphis graminum
  • Trichoderma citrinoviride
  • Bisorbicillinoids
  • Bislongiquinolide and 16,17-dihydrobislongiquinolide
  • Trichodimerol
  • Dihydrotrichodimerol
  • Feeding preference
  • Electrophysiological tests
  • Biocontrol