Skip to main content

Advertisement

SpringerLink
Log in

Metabolome analysis of food-chain between plants and insects

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Evolution has shown the co-dependency between host plants and predators (insects), especially inevitable dependency of predators on plant biomass for securing their energy sources. It was postulated that NAD+ source used for major energy producing pathway is the glycerol-3-phosphate shuttle in insects. Using high throughput metabolomics approach, we found that larva of leaf beetle (Gastrophysa atrocyanea), which feed oxalate-rich plants (Rumex obtusifolius), possessed a unique mechanism for accumulating unusually high amounts of lactate. Similarly, larva of butterfly (Papilio machaon) fed with fennel (Foeniculum vulgare) accumulated lactate. Same butterfly also showed the elevated level of glycerol-3-phosphate equivalent to lactate. These evidences provide new insights into the mechanism underlying metabolite alteration between host plants and insect herbivores.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Candy, D. J., & Kilby, B. A. (1975). Insect biochemistry and function. London/New York: Chapman and hall/Wiley.

    Book  Google Scholar 

  • Dickie, C. W., Hamann, M. H., Carroll, W. D., & Chow, F. (1978). Oxalate (Rumex venosus) poisoning in cattle. Journal of the American Veterinary Medical Association, 173, 73–74.

    CAS  PubMed  Google Scholar 

  • Kaddurah-Daouk, R., Kristal, B. S., & Weinshilboum, R. M. (2008). Metabolomics: A global biochemical approach to drug response and disease. Annual Reviews of Pharmacology and Toxicology, 48, 653–683.

    Article  CAS  Google Scholar 

  • Miyagi, A., Takahara, K., Kasajima, I., Takahashi, H., Kawai-Yamada, M., & Uchimiya, H. (2011). Fate of 13C in metabolic pathways and effects of high CO2 on the alteration of metabolites in Rumex obtusifolius L. Metabolomics, 7, 524–535.

    Article  CAS  Google Scholar 

  • Miyagi, A., Takahashi, H., Takahara, K., Hirabayashi, T., Nishimura, Y., Tezuka, T., et al. (2010a). Principal component and hierarchical clustering analysis of metabolites in destructive weeds; polygonaceous plants. Metabolomics, 6, 146–155.

    Article  CAS  Google Scholar 

  • Miyagi, A., Takahara, K., Takahashi, H., Kawai-Yamada, M., & Uchimiya, H. (2010b). Targeted metabolomics in an intrusive weed, Rumex obtusifolius L., grown under different environmental conditions reveals alterations of organ related metabolite pathway. Metabolomics, 6, 497–510.

    Article  CAS  Google Scholar 

  • Miyagi, A., Uchimiya, M., Kawai-Yamada, M., & Uchimiya, H. (2013a). Impact of aluminium stress in oxalate and other metabolites in Rumex obtusifolius. Weed Research, 53, 30–41.

    Article  CAS  Google Scholar 

  • Miyagi, A., Uchimiya, M., Kawai-Yamada, M. & Uchimiya, H. (2013b). An antagonist treatment in combination with tracer experiments revealed isocitrate pathway dominant to oxalate biosynthesis in Rumex obtusifolius L. Metabolomics, 9, 590–598.

  • Neermann, I., & Wagner, R. (1996). Comparative analysis of glucose and glutamine metabolism in transformed mammalian cell lines, insect and primary liver cells. Journal of Cellular Physiology, 166, 152–169.

    Article  CAS  PubMed  Google Scholar 

  • Nicholson, J. K., Wilson, I. D., & Lindon, J. C. (2011). Pharmacometabonomics as an effector for personalized medicine. Pharmacogenomics, 12, 103–111.

    Article  CAS  PubMed  Google Scholar 

  • Ojima, N., Ikeda, S., Koike, O., Fujita, K., & Suzuki, K. (2005). Continuous rearing of an entomoresource, the leaf beetle, Gastrophysa atrocyanea Motschulsky (Coleoptera: Chrysomelidae) on artificial diets. Applied Entomology and Zoology, 40, 119–124.

    Article  Google Scholar 

  • Panciera, R. J., Martin, T., Burrows, G. E., Taylor, D. S., & Rice, L. E. (1990). Acute oxalate poisoning attributable to ingestion of curly dock (Rumex crispus) in sheep. Journal of the American Veterinary Medical Association, 196, 1981–1984.

    CAS  PubMed  Google Scholar 

  • Pauw, A., Stofberg, J., & Waterman, R. J. (2009). Flies and flowers in Darwin’s race. Evolution, 63, 268–279.

    Article  PubMed  Google Scholar 

  • Pedersen, T. H., Nielsen, O. B., Lamb, G. D., & Stephenson, D. G. (2004). Intracellular acidosis enhances the excitability of working muscle. Science, 305, 1144–1147.

    Article  CAS  PubMed  Google Scholar 

  • Reig, R., Sanz, P., Blanche, C., Fontarnau, R., Dominguez, A., & Corbella, J. (1990). Fatal poisoning by Rumex crispus (curled dock): Pathological findings and application of scanning electron microscopy. Veterinary and Human Toxicology, 32, 468–470.

    CAS  PubMed  Google Scholar 

  • Schauer, N., & Fernie, A. R. (2006). Plant metabolomics: Towards biological function and mechanism. Trends in Plant Sciences, 11, 508–516.

    Article  CAS  Google Scholar 

  • Shulaev, V., Cortes, D., Miller, G., & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, K., Hosaka, M., & Miya, K. (1984). The amino acid pool of Bombyx mori eggs during diapause. Insect Biochemistry, 14, 557–561.

    Article  CAS  Google Scholar 

  • Tanaka, K., Uda, Y., Ono, Y., Nakagawa, T., Suwa, M., Yamaoka, R., et al. (2009). Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Current Biology, 19, 881–890.

    Article  CAS  PubMed  Google Scholar 

  • Toju, H. (2011). Weevils and camellias in a Darwin’s race: Model system for the study of eco-evolutionary interactions between species. Ecological Research, 26, 239–251.

    Article  Google Scholar 

  • Xiao, Y., Wang, Q., Erb, M., Turlings, T. C. J., Ge, L., Hu, L., et al. (2012). Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecological Letters, 15, 1130–1139.

    Article  CAS  Google Scholar 

  • Xu, W. H., Lu, Y. X., & Denlinger, D. L. (2012). Cross-talk between the fat body and brain regulates insect developmental arrest. Proceedings of the National Academy of Sciences of the United Sates of America, 109, 14687–14692.

    Article  CAS  Google Scholar 

  • Zaller, J. G. (2004). Ecology and non-chemical control of Rumex crispus and R. obtusifolius (Polygonaceae): A review. Weed Research, 44, 414–432.

    Article  Google Scholar 

  • Zebe, E. C., & McShan, W. H. (1957). Lactic and alpha-glycerophosphate dehydrogenases in insects. The Journal of General Physiology, 40, 779–790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by a Grant from the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN), and Grants from MEXT, Japan.

Author information

Authors and Affiliations

  1. Institute for Environmental Science and Technology, Saitama University, 225 Shimo-Okubo, Sakura-Ku, Saitama-city, Saitama, 338-8570, Japan

    Atsuko Miyagi, Maki Kawai-Yamada & Hirofumi Uchimiya

  2. Graduate School of Science and Engineering, Saitama University, 225 Shimo-Okubo, Sakura-Ku, Saitama-city, Saitama, 338-8570, Japan

    Maki Kawai-Yamada

  3. USDA-ARS Southern Regional Research Center, 1100 Robert E. Lee Blvd., New Orleans, LA, 70124, USA

    Minori Uchimiya

  4. Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, Miyagi, 980-8577, Japan

    Noriyuki Ojima

  5. Office of Research Exchange, Iwate University, Morioka, Iwate, 020-8550, Japan

    Koichi Suzuki

Authors
  1. Atsuko Miyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maki Kawai-Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Minori Uchimiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noriyuki Ojima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Koichi Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hirofumi Uchimiya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hirofumi Uchimiya.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 164 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miyagi, A., Kawai-Yamada, M., Uchimiya, M. et al. Metabolome analysis of food-chain between plants and insects. Metabolomics 9, 1254–1261 (2013). https://doi.org/10.1007/s11306-013-0542-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11306-013-0542-9

Keywords

Search

Navigation