Slodowicz, M.; Ceriani-Nakamurakare, E.; Carmarán, C.; González-Audino, P. "Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus" (2019) Entomologia Experimentalis et Applicata
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Megaplatypus mutatus (Chapuis) (Coleoptera: Platypodidae) is an ambrosia beetle native to South America that causes economic loss and was recently introduced to Italy, where it attacks and damages live poplar trees. Sulcatol and sulcatone are male-produced pheromone components involved in the mating process of M. mutatus. Their relative proportions are highly variable among insects, although the temporal pattern shows that initially only sulcatol is present, and sulcatone increases with time, until they are finally both depleted. Sulcatol and sulcatone may be produced de novo by the beetles, they may be produced by fungi, or both pathways may contribute to their production. Sulcatol is stored in the males’ hindgut but sulcatone is only present in emissions, so there is an oxidation process to transform the alcohol to the ketone before or during pheromone release. It is our hypothesis that fungi associated with M. mutatus are responsible for this process. In this work, we studied a possible contribution of associated microorganisms in the conversion of sulcatol into sulcatone and its consequent role in the temporal release pattern of these sex pheromone components observed in male insects. Moreover, we inhibited the postulated enzymes involved in this pheromone conversion process – 3-hydroxy-3-methyl-glutatyl-CoA reductase (HMGR) and P450 enzymes of a fungal strain – and added an antibiotic and a fungicide to the homogenate during sulcatol-sulcatone conversion. Among the fungal species, particular interest was given to Graphium basitruncatum (Matsush.) Seifert & Okada (Microascales), as it is present in male but not in female exoskeletons and in insect gallery samples, suggesting a possible different role in pherome production, as the male is the pheromone-producing sex. Several isolated strains were able to convert sulcatol to sulcatone, whereas the fungus G. basitruncatum showed the highest production of this ketone. Additionally, inhibition of P450 enzymes and HMGR from G. basitruncatum on this alcohol-ketone conversion demonstrated that HMGR is involved in sulcatone generation using sulcatol as precursor, and that P450 enzymes are not. Finally, sulcatone production diminished significantly in homogenized tissues of male and female M. mutatus following addition of an antibiotic and a fungicide. The results suggest that fungi associated with M. mutatus are involved in pheromone production. © 2019 The Netherlands Entomological Society


Documento: Artículo
Título:Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus
Autor:Slodowicz, M.; Ceriani-Nakamurakare, E.; Carmarán, C.; González-Audino, P.
Filiación:Centro de Investigaciones de Plagas e Insecticidas, J.B. de La Salle 4397 (B1603ALO), Villa Martelli, Buenos Aires, Argentina
Depto. Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Av. Int. Güiraldes 2620, Buenos Aires, C1428EHA, Argentina
Palabras clave:ambrosia beetle; Coleoptera; Graphium basitruncatum; Platypodidae; poplar tree; sulcatol; sulcatone
Título revista:Entomologia Experimentalis et Applicata
Título revista abreviado:Entomol. Exp. Appl.


  • Alfaro, R.I., Humble, L.M., Gonzalez, P., Villaverde, R., Allegro, G., The threat of the ambrosia beetle Megaplatypus mutatus (Chapuis) (= Platypus mutatus Chapuis) to world poplar resources (2007) Forestry, 80, pp. 471-479. , &
  • Ayres, M.P., Wilkens, R.T., Ruel, J.J., Lombardero, M.J.M.J., Vallery, E., Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi (2000) Ecology, 81, pp. 2198-2210. , &
  • Belan, A., Bolte, J., Fauve, A., Gourcy, J.G., Veschambre, H., Use of biological systems for the preparation of chiral molecules, 3. An application in pheromone synthesis: preparation of sulcatol enantiomers (1987) Journal of Organic Chemistry, 52, pp. 256-260. , &
  • Bleiker, K.P., Six, D.L., Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics (2007) Environmental Entomology, 36, pp. 1384-1396. , &
  • Blomquist, G.J., Figueroa-Teran, R., Aw, M., Song, M., Gorzalski, A., Pheromone production in bark beetles (2010) Insect Biochemistry and Molecular Biology, 40, pp. 699-712
  • Brand, J.M., Bracke, J.W., Britton, L.N., Markovetz, A.J., Barras, S.J., Bark beetle pheromones: production of verbenone by a mycangial fungus of Dendroctonus frontalis (1976) Journal of Chemical Ecology, 2, pp. 195-199. , &
  • van den Brink, H.M., van Gorcom, R.F.M., van den Hondel, C.A.M.J.J., Punt, P.J., Cytochrome P450 enzyme systems in fungi (1998) Fungal Genetics and Biology, 23, pp. 1-17. , &
  • Carrasco Navarro, V., Brozinski, J.M., Leppänen, M.T., Honkanen, J.O., Kronberg, L., Kukkonen, J.V.K., Inhibition of pyrene biotransformation by piperonyl butoxide and identification of two pyrene derivatives in Lumbriculus variegatus (Oligochaeta) (2011) Environmental Toxicology and Chemistry, 30, pp. 1069-1078. , &
  • Ceriani-Nakamurakare, E., Slodowicz, M., Gonzalez-Audino, P., Dolinko, A., Carmarán, C., Mycobiota associated with the ambrosia beetle Megaplatypus mutatus: threat to poplar plantations (2016) Forestry, 89, pp. 191-200. , &
  • Cooperband, M.F., Cossé, A.A., Jones, T.H., Carrillo, D., Cleary, K., Pheromones of three ambrosia beetles in the Euwallacea fornicatus species complex: ratios and preferences (2017) PeerJ, 5
  • Endo, A., A historical perspective on the discovery of statins (2010) Proceedings of the Japan Academy B, 86, pp. 484-493
  • Funes, H., Zerba, E., González-Audino, P., Comparison of three types of traps baited with sexual pheromones for ambrosia beetle Megaplatypus mutatus (Coleoptera: Platypodinae) in poplar plantations (2009) Journal of Economic Entomology, 102, pp. 1546-1550. , &
  • Funes, H., Griffo, R., Zerba, E., Gonzalez-Audino, P., Mating disruption of the ambrosia beetle Megaplatypus mutatus in poplar and hazelnut plantations using reservoir systems for pheromones (2011) Entomologia Experimentalis et Applicata, 139, pp. 226-234. , &
  • Gatti Liguori, P., Zerba, E., Alzogaray, R.A., Gonzalez-Audino, P., 3-Pentanol: a new attractant present in volatile emissions from the ambrosia beetle, Megaplatypus mutatus (2008) Journal of Chemical Ecology, 34, pp. 1446-1451. , &
  • Gatti, P., Zerba, E., Gonzalez-Audino, P., Anatomical site of pheromone accumulation and temporal pattern of pheromone emission in the ambrosia beetle Megaplatypus mutatus (2011) Physiological Entomology, 36, pp. 201-207. , &
  • Gonzalez-Audino, P., Villaverde, R., Alfaro, R., Zerba, E., Identification of volatile emissions from Platypus mutatus (= sulcatus) (Coleoptera: Platypodidae) and their behavioral activity (2005) Journal of Economic Entomology, 98, pp. 1506-1509. , &
  • Griffo, R., Pesapane, G., Funes, H., González-Audino, P., Germinara, G., Diffusione e controllo di platipo in Campania (2012) L'Informatore Agrario, 31, pp. 66-68. , &
  • Harrington, T.C., Ecology and evolution of mycophagous bark beetles and their fungal partners (2005) Insect-Fungal Associations: Ecology and Evolution, pp. 257-291. , (ed. by, FE Vega, &, M Blackwell, Oxford University Press, New York, NY, USA
  • Hopps, H.E., Wisseman, C.L., Hahn, F.E., Smadel, J.E., Ho, R., Mode of action of chloramphenicol IV (1956) Journal of Bacteriology, 72, pp. 561-567. , &
  • Hunt, D.W.A., Borden, J.H., Terpene alcohol pheromone production by Dendroctonus ponderosae and Ips paraconfusus (Coleoptera: Scolytidae) in the absence of readily culturable microorganisms (1989) Journal of Chemical Ecology, 15, pp. 1433-1463. , &
  • Hunt, D.W.A., Borden, J.H., Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae) (1990) Journal of Chemical Ecology, 16, pp. 1385-1397. , &
  • Ivarsson, P., Schlyter, F., Birgersson, G., Demonstration of de novo pheromone biosynthesis in Ips duplicatus (Coleoptera: Scolytidae): inhibition of ipsdienol and E-myrcenol production by compactin (1993) Insect Biochemistry and Molecular Biology, 6, pp. 655-662. , &
  • Klepzig, K.D., Adams, A.S., Handelsman, J., Raffa, K.F., Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans (2009) Environmental Entomology, 38, pp. 67-77. , &
  • Leufvén, A., Bergström, G., Falsen, E., Interconversion of verbenols and verbenone by identified yeasts isolated from the spruce bark beetle Ips typographus (1984) Journal of Chemical Ecology, 10, pp. 1349-1361. , &
  • Matsuzaki, F., Wariishi, H., Functional diversity of cytochrome P450s of the white-rot fungus Phanerochaete chrysosporium (2004) Biochemical and Biophysical Research Communications, 324, pp. 387-393. , &
  • Nes, I.F., Eklund, T., The effect of parabens on DNA, RNA and protein synthesis in Escherichia coli and Bacillus subtilis (1983) Journal of Applied Bacteriology, 54, pp. 237-242. , &
  • Perez, A., Gries, R., Gries, G., Oehlschlager, A.C., Transformation of presumptive precursors to frontalin and exo-brevicomin by bark beetles and west Indian sugarcane weevil (Coleoptera) (1996) Bioorganic & Medicinal Chemistry, 4, pp. 445-450. , &
  • Schmidt-Dannert, C., Biosynthesis of terpenoid natural products in fungi (2015) Advances in Biochemical Engineering/Biotechnology, 148, pp. 19-61
  • Seybold, S.J., Tittiger, C., Biochemistry and molecular biology of de novo isoprenoid pheromone production in the Scolytidae (2003) Annual Review of Entomology, 48, pp. 425-453. , &
  • Seybold, S.J., Vanderwell, D., Biosynthesis and endocrine regulation of pheromone production in the Coleoptera (2003) Insect Pheromone Biochemistry and Molecular Biology: The Biosynthesis and Detection of Pheromones and Plant Volatiles, pp. 137-200. , &, (ed. by, GJ Blomquist, &, RG Vogt, Elsevier Academic Press, San Diego, CA, USA
  • Six, D.L., Ecological and evolutionary determinants of bark beetle – fungus symbioses (2012) Insects, 3, pp. 339-366
  • Slodowicz, M., Ceriani-Nakamurakare, E., Carmarán, C., González Audino, P., Physicochemical properties and field evaluation of monolithic wax formulations for the controlled release of a forest pest pheromone (2017) Journal of Brazilian Chemical Society, 28, pp. 348-359. , &
  • Subramanian, V., Yadav, J.S., Role of P450 monooxygenases in the degradation of the endocrine-disrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium (2009) Applied and Environmental Microbiology, 75, pp. 5570-5580. , &
  • Tittiger, C., Blomquist, G.J., Pheromone biosynthesis in bark beetles (2017) Current Opinion in Insect Science, 24, pp. 68-74. , &
  • Tittiger, C., O'Keeffe, C., Bengoa, C.S., Barkawi, L.S., Seybold, S.J., Blomquist, G.J., Isolation and endocrine regulation of an HMG-CoA synthase cDNA from the male Jeffrey pine beetle, Dendroctonus jeffreyi (Coleoptera: Scolytidae) (2000) Insect Biochemistry and Molecular Biology, 30, pp. 1203-1211. , &
  • Tittiger, C., Barkawi, L.S., Bengoa, C.S., Blomquist, G.J., Seybold, S.J., Structure and juvenile hormone-mediated regulation of the HMG-CoA reductase gene from the Jeffrey pine beetle, Dendroctonus jeffreyi (2003) Molecular and Cellular Endocrinology, 199, pp. 11-21. , &
  • Tokoro, M., Kobayashi, M., Saito, S., Kinuura, H., Nakashima, T., Novel aggregation pheromone, (1S,4R)-p-menth-2-en-1-ol, of the ambrosia beetle, Platypus quercivorus (Coleoptera: Platypodidae) (2007) Bulletin of FFPRI, 6, pp. 49-57
  • Xu, L., Lou, Q., Cheng, C., Lu, M., Sun, J., Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production (2015) Microbial Ecology, 70, pp. 1012-1023. , &
  • Zhao, T., Axelsson, K., Krokene, P., Borg-Karlson, A.-K., Fungal symbionts of the spruce bark beetle synthesize the beetle aggregation pheromone 2-methyl-3-buten-2-ol (2015) Journal of Chemical Ecology, 41, pp. 848-852. , &


---------- APA ----------
Slodowicz, M., Ceriani-Nakamurakare, E., Carmarán, C. & González-Audino, P. (2019) . Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus. Entomologia Experimentalis et Applicata.
---------- CHICAGO ----------
Slodowicz, M., Ceriani-Nakamurakare, E., Carmarán, C., González-Audino, P. "Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus" . Entomologia Experimentalis et Applicata (2019).
---------- MLA ----------
Slodowicz, M., Ceriani-Nakamurakare, E., Carmarán, C., González-Audino, P. "Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus" . Entomologia Experimentalis et Applicata, 2019.
---------- VANCOUVER ----------
Slodowicz, M., Ceriani-Nakamurakare, E., Carmarán, C., González-Audino, P. Sex pheromone component produced by microbial associates of the forest pest Megaplatypus mutatus. Entomol. Exp. Appl. 2019.