Skip to main content
Log in

Specificity of Induction Responses in Sinapis alba L. and Their Effects on a Specialist Herbivore

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

Abstract

The glucosinolate–myrosinase system of Brassicaceae is known to hold a defensive function in both a constitutive and an inducible fashion. Glucosinolates are sulfur- and nitrogen-containing metabolites that are hydrolyzed upon tissue disruption by myrosinase enzymes. The resulting products are toxic for most herbivores. Nevertheless, some insects evolved detoxification mechanisms that enable them to feed exclusively on Brassicaceae. Induction of plant chemical defenses that deter or poison generalists might be ineffective against adapted specialists. We investigated the specificity of short-term induction patterns of chemical defenses in Sinapis alba damaged by a glucosinolate-sequestering specialist herbivore (turnip sawfly, Athalia rosae), a generalist herbivore (fall armyworm, Spodoptera frugiperda), or mechanical wounding (cork borer), and their effects on the behavior of A. rosae. After 24 hr of damage to young leaves, local as well as systemic changes in glucosinolate and myrosinase levels were analyzed. The intensity of the resulting changes was highest in damaged leaves. Induction responses in S. alba were dependent upon the attacking herbivore and were distinct from a mere wound response. Specialist feeding and mechanical wounding evoked up to threefold increases in levels of both parts of the glucosinolate–myrosinase system, whereas generalist feeding induced up to twofold increases in glucosinolate levels only. The majority of constitutive and induced myrosinase activity was found in the insoluble fractions. Possible consequences for the plant–specialist interaction were examined in behavioral tests with larvae and adult females of A. rosae on induced S. alba plants. Larval feeding and adult oviposition patterns were not modulated in relation to plant treatment. Thus, specificity was found in S. alba responses in relation to the inducing agent, but it was not present in return in the effects on the behavior of an adapted herbivore.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

p-OH:

benzylglucosinolate

P :

hydroxybenzylglucosinolate

Fw:

fresh weight of sample

References

  • Agerbirk, N., Müller, C., Olsen, C. E., and Chew, F. S. 2006. A common pathway for metabolism of 4-hydroxybenzylglucosinolate in Pieris and Anthocaris (Lepidoptera: Pieridae). Biochem. Syst. Ecol. 34:189–198.

    Article  CAS  Google Scholar 

  • Agerbirk, N., Olsen, C. E., and Nielsen, J. K. 2001. Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58:91–100.

    Article  PubMed  CAS  Google Scholar 

  • Agrawal, A. A. 2000. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813.

    Google Scholar 

  • Agrawal, A. A. and Kurashige, N. S. 2003. A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J. Chem. Ecol. 29:1403–1415.

    Article  PubMed  CAS  Google Scholar 

  • Andréasson, E., Wretblad, S., Granér, G., Wu, X., Zhang, J., Dixelius, C., Rask, L., and Meijer, J. 2001. The myrosinase-glucosinolate system in the interaction between Leptosphaeria maculans and Brassica napus. Mol. Plant Pathol. 2:281–286.

    Article  Google Scholar 

  • Baldwin, I. T. and Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145.

    Article  CAS  Google Scholar 

  • Barker, A. M., Molotsane, R., Müller, C., Schaffner, U., and Städler, E. 2006. Chemosensory and behavioural responses of the turnip sawfly, Athalia rosae, to glucosinolates and isothiocyanates. Chemoecology 16:209–218.

    Article  CAS  Google Scholar 

  • Bede, J. C., Musser, R. O., Felton, G. W., and Korth, K. L. 2006. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol. Biol. 60:519–531.

    Article  PubMed  CAS  Google Scholar 

  • Bodnaryk, R. P. 1992. Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard. Phytochemistry 31:2671–2677.

    Article  CAS  Google Scholar 

  • Bones, A. M. and Rossiter, J. T. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067.

    Article  PubMed  CAS  Google Scholar 

  • Brader, G., Mikkelsen, M. D., Halkier, B. A., and Palva, E. T. 2006. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 46:758–767.

    Article  PubMed  CAS  Google Scholar 

  • Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72:248–254.

    Article  PubMed  CAS  Google Scholar 

  • Brown, P. D., Tokuhisa, J. G., Reichelt, M., and Gershenzon, J. 2003. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481.

    Article  PubMed  CAS  Google Scholar 

  • Burow, M., Müller, R., Gershenzon, J., and Wittstock, U. 2006. Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. J. Chem. Ecol. 32:2333–2349.

    Article  PubMed  CAS  Google Scholar 

  • Charron, C. S., Saxton, A. M., and Sams, C. E. 2005. Relationship of climate and genotype to seasonal variation in the glucosinolate-myrosinase system. I. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. J. Sci. Food Agric. 85:671–681.

    Article  CAS  Google Scholar 

  • De Vos, M., Van Zaanen, W., Koornneef, A., Korzelius, J. P., Dicke, M., Van Loon, L. C., and Pieterse, C. M. J. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142:352–363.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M. and Hilker, M. 2003. Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl. Ecol. 4:3–14.

    Article  CAS  Google Scholar 

  • Doughty, K. J., Kiddle, G. A., Pye, B. J., Wallsgrove, R. M., and Pickett, J. A. 1995. Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 38:347–350.

    Article  CAS  Google Scholar 

  • Eichenseer, H., Mathews, M. C., Bi, J. L., Murphy, J. B., and Felton, G. W. 1999. Salivary glucose oxidase: Multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42:99–109.

    Article  PubMed  CAS  Google Scholar 

  • Eriksson, S., Andréasson, E., Ekbom, B., Granér, G., Pontoppidan, B., Taipalensuu, J., Zhang, J. M., Rask, L., and Meijer, J. 2002. Complex formation of myrosinase isoenzymes in oilseed rape seeds are dependent on the presence of myrosinase-binding proteins. Plant Physiol. 129:1592–1599.

    Article  PubMed  CAS  Google Scholar 

  • Felton, G. W. and Eichenseer, H. 1999. Herbivore saliva and its effects on plant defense against herbivores and pathogens, pp. 19–36, in A. A. Agrawal, S. Tuzun and E. Bent (eds). Induced Plant Defenses against Pathogens and Herbivores. The American Phytopathological Society, St. Paul, USA.

    Google Scholar 

  • Fordyce, J. A. 2001. The lethal plant defense paradox remains: inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtail. Entomol. Exp. Appl. 100:339–346.

    Article  CAS  Google Scholar 

  • Giamoustaris, A. and Mithen, R. 1995. The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Ann. Appl. Biol. 126:347–363.

    Article  CAS  Google Scholar 

  • Halkier, B. A. and Gershenzon, J. 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant. Biol. 57:303–333.

    Article  PubMed  CAS  Google Scholar 

  • Hartmann, T. and Ober, D. 2000. Biosynthesis and metabolism of pyrrolizidine alkaloids in plants and specialized insect herbivores, pp. 207–243, in F. J. Leeper and J. C. Vederas (eds.). Biosynthesis: Aromatic Polyketides, Isoprenoids, Alkaloids. Springer, Berlin, Germany.

    Google Scholar 

  • Hilker, M. and Meiners, T. 2006. Early herbivore alert: Insect eggs induce plant defense. J. Chem. Ecol. 32:1379–1397.

    Article  PubMed  CAS  Google Scholar 

  • Hopkins, R. J., Ekbom, B., and Henkow, L. 1998a. Glucosinolate content and susceptibility for insect attack of three populations of Sinapis alba. J. Chem. Ecol. 24:1203–1216.

    Article  CAS  Google Scholar 

  • Hopkins, R. J., Griffiths, D. W., Birch, A. N. E., and McKinlay, R. G. 1998b. Influence of increasing herbivore pressure on modification of glucosinolate content of swedes (Brassica napus spp. rapifera). J. Chem. Ecol. 24:2003–2019.

    Article  CAS  Google Scholar 

  • King, E. G. and Leppla, N. C. 1984. Advances and challenges in insect rearing. Agricultural Research Service (Southern Region), US Department of Agriculture, US Government Printing Office, New Orleans, Louisiana, USA.

    Google Scholar 

  • Kleinwächter, M. and Selmar, D. 2004. A novel approach for reliable activity determination of ascorbic acid depending myrosinases. J. Biochem. Biophys. Methods 59:253–265.

    Article  PubMed  CAS  Google Scholar 

  • Koritsas, V. M., Lewis, J. A., and Fenwick, G. R. 1991. Glucosinolate responses of oilseed rape, mustard and kale to mechanical wounding and infestation by cabbage stem flea beetle (Psylliodes chrysocephala). Ann. Appl. Biol. 118:209–221.

    Google Scholar 

  • Kunst, A., Draeger, B., and Ziegenhorn, J. 1984. D-glucose: colorimetric methods with glucose oxidase and peroxidase, pp. 178–185, in H. U. Bergmeyer and M. Graßl (eds). Metabolites 1: Carbohydrates. Verlag Chemie, Weinheim, Germany.

    Google Scholar 

  • Ludwig-Müller, J., Schubert, B., Pieper, K., Ihmig, S., and Hilgenberg, W. 1997. Glucosinolate content in susceptible and resistant Chinese cabbage varieties during development of clubroot disease. Phytochemistry 44:407–414.

    Article  Google Scholar 

  • Martin, N. and Müller, C. 2007. Induction of plant responses by a sequestering insect: Relationship of glucosinolate concentration and myrosinase activity. Basic Appl. Ecol. 8:13–25.

    Article  CAS  Google Scholar 

  • Mithöfer, A., Wanner, G., and Boland, W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137:1160–1168.

    Article  PubMed  CAS  Google Scholar 

  • Moss, D. W. 1984. Nomenclature and units in enzymology, pp. 7–14, in H. U. Bergmeyer and M. Graßl (eds). Fundamentals. Verlag Chemie, Weinheim, Germany.

    Google Scholar 

  • Müller, C., Agerbirk, N., Olsen, C. E., Boevé, J. L., Schaffner, U., and Brakefield, P. M. 2001. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J. Chem. Ecol. 27:2505–2516.

    Article  PubMed  Google Scholar 

  • Müller, C., Boevé, J. L., and Brakefield, P. 2002. Host plant derived feeding deterrence towards ants in the turnip sawfly Athalia rosae. Entomol. Exp. Appl. 104:153–157.

    Article  Google Scholar 

  • Müller, C. and Brakefield, P. M. 2003. Analysis of a chemical defense in sawfly larvae: Easy bleeding targets predatory wasps in late summer. J. Chem. Ecol. 29:2683–2694.

    Article  PubMed  Google Scholar 

  • Müller, C. and Martens, N. 2005. Testing predictions of the ‘evolution of increased competitive ability’ hypothesis for an invasive crucifer. Evol. Ecol. 19:533–550.

    Article  Google Scholar 

  • Müller, C. and Sieling, N. 2006. Effects of glucosinolate and myrosinase levels in Brassica juncea on a glucosinolate-sequestering herbivore—and vice versa. Chemoecology 16:191–201.

    Article  CAS  Google Scholar 

  • Müller, C. and Wittstock, U. 2005. Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae. Insect Biochem. Mol. Biol. 35:1189–1198.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., Williams, S. A., Brown, J. K., and Felton, G. W. 2005. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch. Insect Biochem. Physiol. 58:128–137.

    Article  PubMed  CAS  Google Scholar 

  • Orians, C. 2005. Herbivores, vascular pathways, and systemic induction: facts and artifacts. J. Chem. Ecol. 31:2231–2242.

    Article  PubMed  CAS  Google Scholar 

  • Orians, C. M., Pomerleau, J., and Ricco, R. 2000. Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J. Chem. Ecol. 26:471–485.

    Article  CAS  Google Scholar 

  • Pontoppidan, B., Hopkins, R., Rask, L., and Meijer, J. 2005. Differential wound induction of the myrosinase system in oilseed rape (Brassica napus): contrasting insect damage with mechanical damage. Plant Sci. 168:715–722.

    Article  CAS  Google Scholar 

  • Rask, L., Andréasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., and Meijer, J. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42:93–113.

    Article  PubMed  CAS  Google Scholar 

  • Reymond, P., Bodenhausen, N., Van Poecke, R. M. P., Krishnamurthy, V., Dicke, M., and Farmer, E. E. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.

    Article  PubMed  CAS  Google Scholar 

  • Rostás, M., Bennett, R., and Hilker, M. 2002. Comparative physiological responses in Chinese cabbage induced by herbivory and fungal infection. J. Chem. Ecol. 28:2449–2463.

    Article  PubMed  Google Scholar 

  • Schoonhoven, L. M., Jermy, T., and Loon, J. J. A. V. 1998. Insect-Plant Biology. From Physiology to Evolution. Chapman & Hall, London.

    Google Scholar 

  • Schuster-Gajzágó, I., Kiszter, A. K., Tóth-Márkus, M., Baráth, Á., Márkus-Bednarik, Z., and Czukor, B. 2006. The effect of radio frequency heat treatment on nutritional and colloid-chemical properties of different white mustard (Sinapis alba L.) varieties. Innov. Food Sci. & Emer. Tech. 7:74–79.

    Article  CAS  Google Scholar 

  • Schwachtje, J., Minchin, P. E. H., 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. U.S.A. 103:12935–12940.

    Article  PubMed  CAS  Google Scholar 

  • Siemens, D. H. and Mitchell-Olds, T. 1998. Evolution of pest-induced defenses in Brassica plants: tests of theory. Ecology 79:632–646.

    Google Scholar 

  • Spiteller, D. and Boland, W. 2003. N-(17-acyloxy-acyl)-glutamines: Novel surfactants from oral secretions of lepidopteran larvae. J. Org. Chem. 68:8743–8749.

    Article  PubMed  CAS  Google Scholar 

  • Stranger, B. E. and Mitchell-Olds, T. 2005. Nucleotide variation at the myrosinase-encoding locus, TGG1, and quantitative myrosinase enzyme activity variation in Arabidopsis thaliana. Mol. Ecol. 14:295–309.

    Article  PubMed  CAS  Google Scholar 

  • Viswanathan, D. V. and Thaler, J. S. 2004. Plant vascular architecture and within-plant spatial patterns in resource quality following herbivory. J. Chem. Ecol. 30:531–543.

    Article  PubMed  CAS  Google Scholar 

  • von Dahl, C. C., Havecker, M., Schlogl, R., and Baldwin, I. T. 2006. Caterpillar-elicited methanol emission: a new signal in plant–herbivore interactions? Plant J. 46:948–960.

    Article  CAS  Google Scholar 

  • Wadleigh, R. W. and Yu, S. J. 1988. Detoxification of isothiocyanate allelochemicals by glutathione transferase in three lepidopterous species. J. Chem. Ecol. 14:1279–1288.

    Article  CAS  Google Scholar 

  • Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195–216.

    PubMed  CAS  Google Scholar 

  • Widarto, H. T., Van der Meijden, E., Lefeber, A. W. M., Erkelens, C., Kim, H. K., Choi, Y. H., and Verpoorte, R. 2006. Metabolomic differentiation of Brassica rapa following herbivory by different insect instars using two-dimensional nuclear magnetic resonance spectroscopy. J. Chem. Ecol. 32:2417–2428.

    Article  PubMed  CAS  Google Scholar 

  • Zangerl, A. R. 2003. Evolution of induced plant responses to herbivores. Basic Appl. Ecol. 4:91–103.

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank M. Riederer for making lab space and HPLC equipment available, D. Imes and D. Paltian for help with numerous extractions and the Bayer AG for Spodoptera frugiperda eggs. This research was supported by the Sonderforschungsbereich 567 “Mechanismen der interspezifischen Interaktion von Organismen” of the Deutsche Forschungsgemeinschaft.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caroline Müller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Travers-Martin, N., Müller, C. Specificity of Induction Responses in Sinapis alba L. and Their Effects on a Specialist Herbivore. J Chem Ecol 33, 1582–1597 (2007). https://doi.org/10.1007/s10886-007-9322-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9322-1

Keywords

Navigation