Abstract
Fatty acid amino acid conjugates (FACs) have been found in noctuid as well as sphingid caterpillar oral secretions; in particular, volicitin [N-(17-hydroxylinolenoyl)-L-glutamine] and its biochemical precursor, N-linolenoyl-L-glutamine, are known elicitors of induced volatile emissions in corn plants. These induced volatiles, in turn, attract natural enemies of the caterpillars. In a previous study, we showed that N-linolenoyl-L-glutamine in larval Spodoptera litura plays an important role in nitrogen assimilation which might be an explanation for caterpillars synthesizing FACs despite an increased risk of attracting natural enemies. However, the presence of FACs in lepidopteran species outside these families of agricultural interest is not well known. We conducted FAC screening of 29 lepidopteran species, and found them in 19 of these species. Thus, FACs are commonly synthesized through a broad range of lepidopteran caterpillars. Since all FAC-containing species had N-linolenoyl-L-glutamine and/or N-linoleoyl-L-glutamine in common, and the evolutionarily earliest species among them had only these two FACs, these glutamine conjugates might be the evolutionarily older FACs. Furthermore, some species had glutamic acid conjugates, and some had hydroxylated FACs. Comparing the diversity of FACs with lepidopteran phylogeny indicates that glutamic acid conjugates can be synthesized by relatively primitive species, while hydroxylation of fatty acids is limited mostly to larger and more developed macrolepidopteran species.
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Abbreviations
- FACs:
-
fatty acid amino acid conjugates
- VOC:
-
volatile organic compounds
- ESI:
-
electrospray ionization
References
Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276: 945–949.
Alborn, H. T., Brennan, M. M., and Tumlinson, J. H. 2003. Differential activity and degradation of plant volatile elicitors in regurgitant of tobacco hornworm (Manduca sexta) larvae. J. Chem. Ecol. 29:1357–1372.
Alborn, H. T., Hansen, T. V., Jones, T. H., Bennett, D. C., Tumlinson, J. H., Schmelz, E. A., and Teal, P. E. A. 2007. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc. Natl. Acad. Sci. USA 104:12976–12981.
Aboshi, T., Yoshinaga, N., Noge, K., Nishida, R., and Mori, N. 2007. Efficient incorporation of unsaturated fatty acids into volicitin-related compounds in Spodoptera litura (Lepidoptera: Noctuidae). Biosci. Biotech. Biochem. 71:607–610.
De Moraes, C. M., and Mescher, M. C. 2004. Biochemical crypsis in the avoidance of natural enemies by an insect herbivore. Proc. Natl. Acad. Sci. USA 101:8993–8997.
Frey, M., Stettner, C., Paré, P. W., Schmelz, E. A., Tumlinson, J. H., and Gierl, A. 2000. An herbivore elicitor activates the gene for indole emission in maize. Proc. Natl. Acad. Sci. USA 96:14801–14806.
Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol. 125:711–717.
Ishikawa, C., Yoshinaga, N., Aboshi, T., Nishida, R., and Mori, N. 2009. Efficient incorporation of free oxygen into volicitin in Spodoptera litura common cutworm larvae. Biosci. Biotech. Biochem. 73:1883–1885.
Kessler, A., and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.
Li, W., Schuler, M. A., and Berenbaum, M. R. 2003. Diversification of furanocoumarin-metabolizing cytochrome P450 monooxygenases in two papilionids: Specificity and substrate encounter rate. Proc. Natl. Acad. Sci. USA 100:14593–14598.
Mori, N., Alborn, H. T., Teal, P. E. A., and Tumlinson, J. H. 2001. Enzymatic decomposition of elicitors of plant volatiles in Heliothis virescens and Helicoverpa zea. J. Insect Physiol. 47:749–757.
Mori, N., Yoshinaga, N., Sawada, Y., Fukui, M., Shimoda, M., Fujisaki, K., Nishida, R., and Kuwahara, Y. 2003. Identification of volicitin-related compounds from the regurgitant of lepidopteran caterpillars. Biosci. Biotech. Biochem. 67:1168–1171.
Paré, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Concerted biosynthesis of an insect elicitor of plant volatiles. Proc. Natl. Acad. Sci. USA 95:13971–13975.
Pohnert, G., Jung, V., Haukioja, E., Lempa, K., and Bolnad, W. 1999. New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars. Tetrahedron 55:11275–11280.
Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S.M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA 103: 8894–8899.
Schmelz, E. A., Engelberth, J., Alborn, H. T., Tumlinson, J. H., and Teal, P. E. A. 2009. Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc. Natl. Acad. Sci. USA 106:653–657.
Shen, B., Zheng, Z., and Dooner, H. K. 2000. A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proc. Natl. Acad. Sci. USA 97:14807–14812.
Suckling, D. M., Burnip, G. M., Gibb, A. R., Daly, J. M., and Armstrong, K. F. 2001. Host and host plant influences on the leafroller parasitoid Dolichogenidia tasmanica (Braconidae). Entomol. Exp. Appl. 100:253–260.
Truitt, C. L., and Paré, P. W. 2004. In situ translocation of volicitin by beet armyworm larvae to maize and systemic immobility of the herbivore elicitor in planta. Planta 218:999–1007.
Truitt, C. L., Wei, H. X., and Paré, P. W. 2004. A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. The Plant Cell 16:523–532.
Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253.
Yoshinaga, N., Morigaki, N., Matsuda, F., Nishida., R., and Mori, N. 2005. In vitro biosynthesis of volicitin in Spodoptera litura. Insect Biochem. Mol. Biol. 35:175–184.
Yoshinaga, N., Aboshi, T., Ishikawa, C., Fukui, M., Shimoda, M., Nishida, R., Lait, C. G., Tumlinson, J. H., and Mori, N. 2007. Fatty acid amides, previously identified in caterpillars, found in the cricket Teleogryllus taiwanemma and fruit fly Drosophila melanogaster larvae. J. Chem. Ecol. 33:1376–1381.
Yoshinaga, N., Aboshi, T., Abe, H., Nishida, R., Alborn, H. T., Tumlinson, J. H., and Mori, N. 2008. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc. Natl. Acad. Sci. USA 105:18058–18063.
Acknowledgement
We thank Drs. Fujisaki, K., Ando, T., Kunimi, Y., Ichida, M., and Shimoda, M. for providing insect materials. This study was supported partly by Grants-in-aid for Scientific Research (no. 15580090, 18580053, and 19580122) and by the 21st century COE program for Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences from the Ministry of Education, Culture, Sports, Science and Technology of Japan. N.Y. was supported by a Postdoctoral Fellowship for Research Abroad from the Japan Society for the Promotion of Science.
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Yoshinaga, N., Alborn, H.T., Nakanishi, T. et al. Fatty Acid-amino Acid Conjugates Diversification in Lepidopteran Caterpillars. J Chem Ecol 36, 319–325 (2010). https://doi.org/10.1007/s10886-010-9764-8
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DOI: https://doi.org/10.1007/s10886-010-9764-8