Skip to main content
SpringerLink
Log in

Phaseoloidin, a Homogentisic Acid Glucoside from Nicotiana Attenuata Trichomes, Contributes to the Plant’s Resistance against Lepidopteran Herbivores

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plant trichomes are known for their capability to produce and store secondary metabolites that protect plants from biotic and abiotic stresses. 1H NMR studies on intact individual trichomes located on the leaf surface of Nicotiana attenuata revealed the presence of two major secondary metabolites: nicotine, the signature metabolite of the genus, and phaseoloidin, a homogentisic acid glucoside. This glucoside was reported originally from the seeds of Entada phaseoloides, and this is the first report of its occurrence in a Solanaceous plant. Artificial diet feeding bioassays with Manduca sexta and Spodoptera littoralis larvae, two important herbivores of N. attenuata, revealed that the ingestion of phaseoloidin negatively influenced caterpillar performance. This effect was more pronounced for the generalist, S. littoralis, than for the specialists, M. sexta.

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

Similar content being viewed by others

References

  • Arrendale, R. F., Severson, R. F., Sisson, V. A., Costello, C. E., Leary, J. A., Himmelsbach, D. S., and Vanhalbeek, H. 1990. Characterization of the sucrose ester fraction from Nicotiana glutinosa. J. Agric. Food Chem. 38:75–85.

    Article  CAS  Google Scholar 

  • Baldwin, I. T. 1989. Mechanism of damage-induced alkaloid production in wild tobacco. J. Chem. Ecol. 15:1661–1680.

    Article  CAS  Google Scholar 

  • Barua, A. K., Chakrabarty, M., Datta, P. K., and Ray, S. 1988. Phaseoloidin, a homgentisic acid glucoside from Entada phaseoloides. Phytochemistry 27:3259–3261.

    Article  CAS  Google Scholar 

  • Cardoso, M. Z. 2008. Herbivore handling of a plants trichome: The case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae). Neotrop. Entomol. 37:247–252.

    Article  PubMed  Google Scholar 

  • Chortyk, O. T., Kays, S. J., and Teng, Q. 1997. Characterization of insecticidal sugar esters of Petunia. J. Agric. Food Chem. 45:270–275.

    Article  CAS  Google Scholar 

  • Dai, X., Wang, G., Yang, D. S., Tang, Y., Broun, P., Marks, M. D., Sumner, L. W., Dixon, R. A., and Zhao, P. X. 2010. TrichOME: A comparative omics database for plant trichomes. Plant Physiol. 152:44–54.

    Article  PubMed  CAS  Google Scholar 

  • Duke, M. V., Paul, R. N., Elsohly, H. N., Sturtz, G., and Duke, S. O. 1994. Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua. Int. J. Plant Sci. 155:365–372.

    Article  Google Scholar 

  • Duke, S. O., Canel, C., Rimando, A. M., Telle, M. R., Duke, M. V., and Paul, R. N. 2000. Current and potential exploitation of plant glandular trichome productivity. Adv. Bot. Res.: Academic Press. p 121–151.

  • Goodspeed, T. H. 1955. The Genus Nicotiana. New York, Stechert-Hafner, Inc.

    Google Scholar 

  • Heiling, S., Schuman, M. C., Schoettner, M., Mukerjee, P., Berger, B., Schneider, B., Jassbi, A. R., and Baldwin, I. T. 2010. Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-Hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22:273–292.

    Article  PubMed  CAS  Google Scholar 

  • Jones, D., Jones, G. A., Hagen, T., and Creech, E. 1985. Wild species of Nicotiana as a new source of tobacco resistance to the tobacco hornworm Manduca sexta. Entomol. Exp. Appl. 38:157–164.

    Article  Google Scholar 

  • Krügel, T., Lim, M., Gase, K., Halitschke, R., and Baldwin, I. T. 2002. Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12:177–183.

    Article  Google Scholar 

  • Laue, G., Preston, C. A., and Baldwin, I. T. 2000. Fast track to the trichome: Induction of N-acyl nornicotines precedes nicotine induction in Nicotiana repanda. Planta 210:510–4.

    Article  PubMed  CAS  Google Scholar 

  • McKenzie, C. L. and Puterka, G. J. 2004. Effect of sucrose octanoate on survival of nymphal and adult Diaphorina citri (Homoptera: Psyllidae). J. Econ. Entomol. 97:970–975.

    Article  PubMed  CAS  Google Scholar 

  • Moran, G. R. 2005. 4-Hydroxyphenylpyruvate dioxygenase. Arch. Biochem. Biophysics 433:117–128.

    Article  CAS  Google Scholar 

  • Morita, M., Shitan, N., Sawada, K., Van Montagu, M. C. E., Inzé, D., Rischer, H., Goossens, A., Oksman-Caldentey, K.-M., Moriyama, Y., and Yazaki, K. 2009. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc. Natl. Acad. Sci. USA 106:2447–2452.

    Article  PubMed  CAS  Google Scholar 

  • Puterka, G. J., Farone, W., Palmer, T., and Barrington, A. 2003. Structure-function relationships affecting the insecticidal and miticidal activity of sugar esters. J. Econ. Entomol. 96:636–44.

    Article  PubMed  CAS  Google Scholar 

  • Roda, A. L., Oldham, N. J., Svatos, A., and Baldwin, I. T. 2003. Allometric analysis of the induced flavonols on the leaf surface of wild tobacco (Nicotiana attenuata). Phytochemistry 62:527–36.

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller, A. L., Last, R. L., and Pichersky, E. 2008. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J. 54:702–11.

    Article  PubMed  CAS  Google Scholar 

  • Schwachtje, J., Minchin, P. E., Jahnke, S., Van Dongen, J. T., Schittko, U., and Baldwin, I. T. 2006. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. USA 103:12935–40.

    Article  PubMed  CAS  Google Scholar 

  • Shoji, T., Yamada, Y., and Hashimoto, T. 2000. Jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant Cell Physiol. 41:831–839.

    Article  PubMed  CAS  Google Scholar 

  • Sirikantaramas, S., Taura, F., Tanaka, Y., Ishikawa, Y., Morimoto, S., and Shoyama, Y. 2005. Tetrahydrocannabinolic acid synthase, the enzyme controlling marijuana psychoactivity, is secreted into the storage cavity of the glandular trichomes. Plant Cell Physiol. 46:1578–1582.

    Article  PubMed  CAS  Google Scholar 

  • Sirikantaramas, S., Yamazaki, M., and Saito, K. 2008. Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochem. Rev. 7:467–477.

    Article  CAS  Google Scholar 

  • Van Schie, C. C., Haring, M. A., and Schuurink, R. C. 2007. Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol. Biol. 64:251–63.

    Article  PubMed  CAS  Google Scholar 

  • Waldbauer, G. P., Yamamoto, R. T., and Bowers, W. S. 1964. Laboratory rearing of tobacco hornworm Protoparce sexta (Lepidoptera: Sphingidae). J. Econ. Entomol. 57:93-95.

    Google Scholar 

  • Weinhold, A. and Baldwin, I. T. 2011. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl. Acad. Sci. USA 108:7855–7859.

    Article  PubMed  CAS  Google Scholar 

  • Zador, E. and Jones, D. 1986. The biosynthesis of a novel nicotine alkaloid in the trichomes of Nicotiana stocktonii. Plant Physiol. 82:479–84.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank three anonymous reviewers for their comments and the Max Planck Society for funding.

Author information

Author notes

  1. Kamel Shaker

    Present address: Chemistry Department, Faculty of Science, King Khalid University, P. Box: 9004, Abha, Kingdom of Saudi Arabia

Authors and Affiliations

  1. Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745, Jena, Germany

    Alexander Weinhold, Michael Wenzler, Bernd Schneider & Ian T. Baldwin

Authors
  1. Alexander Weinhold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kamel Shaker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Wenzler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernd Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ian T. Baldwin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ian T. Baldwin.

Additional information

Alexander Weinhold, Kamel Shaker, and Michael Wenzler contributed equally to the results presented in this paper.

Electronic Supplementary Materials

Below is the link to the electronic supplementary material.

Supplemental Figure S1

Light micrographs of intact glandular trichomes of Nicotiana attenuata WT leaves. A Two different trichome types are found on the leaf surface, short trichomes with a stem consisting of two to four cells and a multi cellular head (type D), as well as tall trichomes with a multi cellular base, a stem (six to ten cells) and a small head (type C). The short trichomes are found mainly on the leaf surface whereas the tall ones are mostly located on the leaf veins shown in C, where they are even larger than on the surface. Magnification (200x) of a type D trichome B and of the head of a type C trichome (100×) D reveal green structures in the heads, most likely chloroplasts, as described for N. tabacum. E Trichomes of the insertional mutant irGAL83 are characterized by their enlarged basal cells. (JPEG 0 kb)

High resolution image (TIFF 970 kb)

Supplemental Figure S2

Phaseoloidin contents in the trichomes of the insertional mutant irGAL83 and the Nicotiana attenuata wild type line do not differ. Two excised leaves were gently frozen over liquid nitrogen. The trichomes were harvested by gently scratching the leaf surface with a microscope cover slip. The plate was rinsed with 10 ml methanol. Afterwards the extract was concentrated to 1 ml under a constant flow of nitrogen. After centrifuging, the supernatant was transferred to HPLC vials. Phaseoloidin content was analyzed by LC-TOF-MS. Error bars indicate standard errors (WT N = 4; insertional mutant N = 3). (PDF 70.3 kb)

Supplemental Figure S3

Aliphatic part of the NMR spectra from the type C and D trichome samples. The spectrum of D Head contains much more sugar and fatty acid signals, belonging to acyl sugars, than the spectra of C Tip and C Middle. (PDF 96.0 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weinhold, A., Shaker, K., Wenzler, M. et al. Phaseoloidin, a Homogentisic Acid Glucoside from Nicotiana Attenuata Trichomes, Contributes to the Plant’s Resistance against Lepidopteran Herbivores. J Chem Ecol 37, 1091–1098 (2011). https://doi.org/10.1007/s10886-011-0012-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-0012-7

Key Words

Search

Navigation