Skip to main content

Advertisement

Log in

Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore

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

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.

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

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ehrlich P, Raven P (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates amoung plants. Phytochemistry 56:5–51

    Article  CAS  PubMed  Google Scholar 

  • Fraenkel GS (1959) The raison d’Etre of secondary plant substances. Science 129:1466–1470

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kazana E, Pope TW, Tibbles L et al (2007) The cabbage aphid: a walking mustard oil bomb. Proc Biol Sci 274:2271–2277

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Kroymann J, Brown P et al (2001a) Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol 126:811–825

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Macleod AJ, Rossiter JT (1986) Non-enzymatic degradation of 2-hydroxybut-3-. Phytochemistry 25:855–858

    Article  CAS  Google Scholar 

  • Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defense paradox. Entomol Exp Appl 80:193–196

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mithen R (2001) Glucosinolates–biochemistry, genetics and biological activity. Plant Growth Regul 34:91–103

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rossiter JT, James DC, Atkins N (1990) Biosynthesis of 2-hydroxy-3-butenylglucosinolate 3-butenylglucosinolate in Brassica napus. Phytochemistry 29:2509–2512

    Article  CAS  Google Scholar 

  • Spiller NJ, Koenders L, Tjallingii WF (1990) Xylem ingestion by aphids - a strategy for maintaining water balance. Entomol Exp Appl 55:101–104

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Züst T, Heichinger C, Grossniklaus U et al (2012) Natural enemies drive geographic variation in plant defenses. Science 338(6108):116–119

    Article  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Dave J. Hodgson.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0634-2

Keywords

Navigation