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.
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.
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.
Agrawal, A. A. 2000. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813.
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.
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.
Baldwin, I. T. and Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145.
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.
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.
Bodnaryk, R. P. 1992. Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard. Phytochemistry 31:2671–2677.
Bones, A. M. and Rossiter, J. T. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067.
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.
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.
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.
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.
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.
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.
Dicke, M. and Hilker, M. 2003. Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl. Ecol. 4:3–14.
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.
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.
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.
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.
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.
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.
Halkier, B. A. and Gershenzon, J. 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant. Biol. 57:303–333.
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.
Hilker, M. and Meiners, T. 2006. Early herbivore alert: Insect eggs induce plant defense. J. Chem. Ecol. 32:1379–1397.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Orians, C. 2005. Herbivores, vascular pathways, and systemic induction: facts and artifacts. J. Chem. Ecol. 31:2231–2242.
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.
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.
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.
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.
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.
Schoonhoven, L. M., Jermy, T., and Loon, J. J. A. V. 1998. Insect-Plant Biology. From Physiology to Evolution. Chapman & Hall, London.
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.
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.
Siemens, D. H. and Mitchell-Olds, T. 1998. Evolution of pest-induced defenses in Brassica plants: tests of theory. Ecology 79:632–646.
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.
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.
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.
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.
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.
Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195–216.
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.
Zangerl, A. R. 2003. Evolution of induced plant responses to herbivores. Basic Appl. Ecol. 4:91–103.
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
Corresponding author
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-007-9322-1