Abstract
In some plant-insect interactions, specialist herbivores exploit the chemical defenses of their food plant to their own advantage. Brassica plants produce glucosinolates that are broken down into defensive toxins when tissue is damaged, but the specialist aphid, Brevicoryne brassicae, uses these chemicals against its own natural enemies by becoming a “walking mustard-oil bomb”. Analysis of glucosinolate concentrations in plant tissue and associated aphid colonies reveals that not only do aphids sequester glucosinolates, but they do so selectively. Aphids specifically accumulate sinigrin to high concentrations while preferentially excreting a structurally similar glucosinolate, progoitrin. Surveys of aphid infestation in wild populations of Brassica oleracea show that this pattern of sequestration and excretion maps onto host plant use. The probability of aphid infestation decreases with increasing concentrations of progoitrin in plants. Brassica brassicae, therefore, appear to select among food plants according to plant secondary metabolite profiles, and selectively store only some compounds that are used against their own enemies. The results demonstrate chemical and behavioral mechanisms that help to explain evidence of geographic patterns and evolutionary dynamics in Brassica-aphid interactions.
Similar content being viewed by others
References
Abdalsamee MK, Müller C (2012) Effects of indole glucosinolates on performance and sequestration by the sawfly Athalia rosae and consequences of feeding on the plant defense system. J Chem Ecol 38:1366–1375
Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant–insect interactions. Curr Opin Plant Biol 4:351–358
Barbieri G, Pernice R, Maggio A et al (2008) Glucosinolates profile of Brassica rapa L. subsp. Sylvestris L. Janch. var. esculenta Hort. Food Chem 107:1687–1691
Beran F, Pauchet Y, Kunert G et al (2014) Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system. Proc Natl Acad Sci U S A 111:7349–7354
Bridges M, Jones AME, Bones AM et al (2002) Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc Biol Sci 269:187–191
Ehrlich P, Raven P (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608
Fabre N, Poinsot V, Debrauwer L et al (2007) Characterisation of glucosinolates using electrospray ion trap and electrospray quadrupole time-of-flight mass spectrometry. Phytochem Anal 18:306–319
Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates amoung plants. Phytochemistry 56:5–51
Fraenkel GS (1959) The raison d’Etre of secondary plant substances. Science 129:1466–1470
Francis F, Lognay G, Wathelet JP, Haubruge E (2001) Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J Chem Ecol 27:243–256
Francis F, Lognay G, Wathelet JP, Haubruge E (2002) Characterisation of aphid myrosinase and degradation studies of glucosinolates. Arch Insect Biochem Physiol 50:173–182
Gabrys B, Tjallingii WF, Van Beek TA (1997) Analysis of EPG recorded probing by cabbage aphid on host plant parts with different glucosinolate contents. J Chem Ecol 23:1661–1673
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333
Jones AME, Bridges M, Bones AM et al (2001) Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). Insect Biochem Mol Biol 31:1–5
Kazana E, Pope TW, Tibbles L et al (2007) The cabbage aphid: a walking mustard oil bomb. Proc Biol Sci 274:2271–2277
Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019
Kim JH, Lee BW, Schroeder FC, Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54:1015–1026
Kliebenstein DJ, Kroymann J, Brown P et al (2001a) Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol 126:811–825
Kliebenstein DJ, Lambrix VM, Reichelt M et al (2001b) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:681–693
Kliebenstein DJ, Kroymann J, Mitchell-Olds T (2005) The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol 8:264–271
Koroleva OA, Davies A, Deeken R et al (2000) Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk. Plant Physiol 124:599–608
Kos M, Broekgaarden C, Kabouw P et al (2011) Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea. Funct Ecol 25:1113–1124
Kos M, Houshyani B, Achhami BB et al (2012) Herbivore-mediated effects of glucosinolates on different natural enemies of a specialist aphid. J Chem Ecol 38:100–115
Macleod AJ, Rossiter JT (1986) Non-enzymatic degradation of 2-hydroxybut-3-. Phytochemistry 25:855–858
Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defense paradox. Entomol Exp Appl 80:193–196
Malcolm SB, Cockrell BJ, Brower LP (1989) Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. J Chem Ecol 15:819–853
Mellon FA, Bennett RN, Holst B, Williamson G (2002) Intact glucosinolate analysis in plant extracts by programmed cone voltage electrospray LC/MS: performance and comparison with LC/MS/MS methods. Anal Biochem 306:83–91
Mithen R (2001) Glucosinolates–biochemistry, genetics and biological activity. Plant Growth Regul 34:91–103
Mohn T, Cutting B, Ernst B, Hamburger M (2007) Extraction and analysis of intact glucosinolates - a validated pressurized liquid extraction/liquid chromatography-mass spectrometry protocol for Isatis tinctoria, and qualitative analysis of other cruciferous plants. J Chromatogr A 1166:142–151
Nishida R (2002) Sequestration of defensive substances. Annu Rev Entomol 57–92
Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154
Pentzold S, Zagrobelny M, Rook F, Bak S (2014) How insects overcome two-component plant chemical defense: plant β-glucosidases as the main target for herbivore adaptation. Biol Rev 89:531–551
Pontoppidan B, Hopkins R, Rask L, Meijer J (2003) Infestation by cabbage aphid (Brevicoryne brassicae) on oilseed rape (Brassica napus) causes a long lasting induction of the myrosinase system. Entomol Exp Appl 109:55–62
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rochfort SJ, Trenerry VC, Imsic M et al (2008) Class targeted metabolomics: ESI ion trap screening methods for glucosinolates based on MSn fragmentation. Phytochemistry 69:1671–1679
Rossiter JT, James DC, Atkins N (1990) Biosynthesis of 2-hydroxy-3-butenylglucosinolate 3-butenylglucosinolate in Brassica napus. Phytochemistry 29:2509–2512
Spiller NJ, Koenders L, Tjallingii WF (1990) Xylem ingestion by aphids - a strategy for maintaining water balance. Entomol Exp Appl 55:101–104
Tian Q, Rosselot RA, Schwartz SJ (2005) Quantitative determination of intact glucosinolates in broccoli, broccoli sprouts, Brussels sprouts, and cauliflower by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry. Anal Biochem 343:93–99
Velasco P, Soengas P, Vilar M et al (2008) Comparison of glucosinolate profiles in leaf and seed tissues of different Brassica napus crops. J Am Soc Hortic Sci 133:551–558
Venables WN, Ripley BD (2002) Modern Applied Statistics with S. 4th edn. Springer, New York
Winde I, Wittstock U (2011) Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry 72:1566–1575
Wittstock U, Agerbirk N, Stauber EJ et al (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101:4859–4864
Züst T, Heichinger C, Grossniklaus U et al (2012) Natural enemies drive geographic variation in plant defenses. Science 338(6108):116–119
Acknowledgments
The authors thank Peter Behrens for access to Prussia Cove field sites. NG was funded by the European Social Fund, the British Mass Spectrometry Society, and DH by the Natural Environment Research Council.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Fig. 1
(PDF 3 kb)
ESM 1
(DOCX 20 kb)
Rights and permissions
About this article
Cite this article
Goodey, N.A., Florance, H.V., Smirnoff, N. et al. Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore. J Chem Ecol 41, 956–964 (2015). https://doi.org/10.1007/s10886-015-0634-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-015-0634-2