Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae

Müller C, Agerbirk N, Olsen CE, Boevé J-L, Schaffner U, Brakefield PM (2001)
Journal of Chemical Ecology 27(12): 2505-2516.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Müller, CarolineUniBi; Agerbirk, Niels; Olsen, Carl Erik; Boevé, Jean-Luc; Schaffner, Urs; Brakefield, Paul M.
Abstract / Bemerkung
Interactions between insects and glucosinolate-containing plant species have been investigated for a long time. Although the glucosinolate–myrosinase system is believed to act as a defense mechanism against generalist herbivores and fungi, several specialist insects use these secondary metabolites for host plant finding and acceptance and can handle them physiologically. However, sequestration of glucosinolates in specialist herbivores has been less well studied. Larvae of the turnip sawfly Athalia rosae feed on several glucosinolate-containing plant species. When larvae are disturbed by antagonists, they release one or more small droplets of hemolymph from their integument. This “reflex bleeding” is used as a defense mechanism. Specific glucosinolate analysis, by conversion to desulfoglucosinolates and analysis of these by high-performance liquid chromatography coupled to diode array UV spectroscopy and mass spectrometry, revealed that larvae incorporate and concentrate the plant's characteristic glucosinolates from their hosts. Extracts of larvae that were reared on Sinapis alba contained sinalbin, even when the larvae were first starved for 22 hr and, thus, had empty guts. Hemolymph was analyzed from larvae that were reared on either S. alba, Brassica nigra, or Barbarea stricta. Leaves were analyzed from the same plants the larvae had fed on. Sinalbin (from S. alba), sinigrin (B. nigra), or glucobarbarin and glucobrassicin (B. stricta) were present in leaves in concentrations less than 1 μmol/g fresh weight, while the same glucosinolates could be detected in the larvae's hemolymph in concentrations between 10 and 31 μmol/g fresh weight, except that glucobrassicin was present only as a trace. In larval feces, only trace amounts of glucosinolates (sinalbin and sinigrin) could be detected. The glucosinolates were likewise found in freshly emerged adults, showing that the sequestered phytochemicals were transferred through the pupal stage.
Journal of Chemical Ecology
Page URI


Müller C, Agerbirk N, Olsen CE, Boevé J-L, Schaffner U, Brakefield PM. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology. 2001;27(12):2505-2516.
Müller, C., Agerbirk, N., Olsen, C. E., Boevé, J. - L., Schaffner, U., & Brakefield, P. M. (2001). Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology, 27(12), 2505-2516. doi:10.1023/A:1013631616141
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. Journal of Chemical Ecology 27, 2505-2516.
Müller, C., et al., 2001. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology, 27(12), p 2505-2516.
C. Müller, et al., “Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae”, Journal of Chemical Ecology, vol. 27, 2001, pp. 2505-2516.
Müller, C., Agerbirk, N., Olsen, C.E., Boevé, J.-L., Schaffner, U., Brakefield, P.M.: Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology. 27, 2505-2516 (2001).
Müller, Caroline, Agerbirk, Niels, Olsen, Carl Erik, Boevé, Jean-Luc, Schaffner, Urs, and Brakefield, Paul M. “Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae”. Journal of Chemical Ecology 27.12 (2001): 2505-2516.

57 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Slow-growth high-mortality: A meta-analysis for insects.
Chen KW, Chen Y., Insect Sci 25(2), 2018
PMID: 27604698
Seasonal and herbivore-induced dynamics of foliar glucosinolates in wild cabbage (Brassica oleracea).
Gols R, van Dam NM, Reichelt M, Gershenzon J, Raaijmakers CE, Bullock JM, Harvey JA., Chemoecology 28(3), 2018
PMID: 29904237
Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels.
Robert CA, Zhang X, Machado RA, Schirmer S, Lori M, Mateo P, Erb M, Gershenzon J., Elife 6(), 2017
PMID: 29171835
Glucosinolates from Host Plants Influence Growth of the Parasitic Plant Cuscuta gronovii and Its Susceptibility to Aphid Feeding.
Smith JD, Woldemariam MG, Mescher MC, Jander G, De Moraes CM., Plant Physiol 172(1), 2016
PMID: 27482077
Suppression of Verticillium dahliae by glucosinolate-containing seed meal amendments
Neubauer C, Hüntemann K, Heitmann B, Müller C., Eur J Plant Pathol 142(2), 2015
PMID: IND601244739
Uncovering different parameters influencing florivory in a specialist herbivore
ABDALSAMEE MK, MÜLLER C., Ecol Entomol 40(3), 2015
PMID: IND601326117
Enemies lost: parallel evolution in structural defense and tolerance to herbivory of invasive Jacobaea vulgaris
Lin T, Doorduin L, Temme A, Pons TL, Lamers GEM, Anten NPR, Vrieling K., Biol Invasions 17(8), 2015
PMID: IND604393734
Taste detection of the non-volatile isothiocyanate moringin results in deterrence to glucosinolate-adapted insect larvae.
Müller C, van Loon J, Ruschioni S, De Nicola GR, Olsen CE, Iori R, Agerbirk N., Phytochemistry 118(), 2015
PMID: 26318325
Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system.
Beran F, Pauchet Y, Kunert G, Reichelt M, Wielsch N, Vogel H, Reinecke A, Svatoš A, Mewis I, Schmid D, Ramasamy S, Ulrichs C, Hansson BS, Gershenzon J, Heckel DG., Proc Natl Acad Sci U S A 111(20), 2014
PMID: 24799680
Glycoalkaloids of wild and cultivated Solanum: effects on specialist and generalist insect herbivores.
Altesor P, García Á, Font E, Rodríguez-Haralambides A, Vilaró F, Oesterheld M, Soler R, González A., J Chem Ecol 40(6), 2014
PMID: 24863489
Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially.
Sewelam N, Jaspert N, Van Der Kelen K, Tognetti VB, Schmitz J, Frerigmann H, Stahl E, Zeier J, Van Breusegem F, Maurino VG., Mol Plant 7(7), 2014
PMID: 24908268
Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae.
Gloss AD, Vassão DG, Hailey AL, Nelson Dittrich AC, Schramm K, Reichelt M, Rast TJ, Weichsel A, Cravens MG, Gershenzon J, Montfort WR, Whiteman NK., Mol Biol Evol 31(9), 2014
PMID: 24974374
Invertebrate and avian predators as drivers of chemical defensive strategies in tenthredinid sawflies.
Boevé JL, Blank SM, Meijer G, Nyman T., BMC Evol Biol 13(), 2013
PMID: 24041372
Host shifts from Lamiales to Brassicaceae in the sawfly genus Athalia.
Opitz SE, Boevé JL, Nagy ZT, Sonet G, Koch F, Müller C., PLoS One 7(4), 2012
PMID: 22485146
Flavonoid metabolites in the hemolymph of European pine sawfly (Neodiprion sertifer) larvae.
Vihakas M, Tähtinen P, Ossipov V, Salminen JP., J Chem Ecol 38(5), 2012
PMID: 22527054
Engineering glucosinolates in plants: current knowledge and potential uses.
Baskar V, Gururani MA, Yu JW, Park SW., Appl Biochem Biotechnol 168(6), 2012
PMID: 22983743
Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae.
Higginson AD, Delf J, Ruxton GD, Speed MP., J Anim Ecol 80(2), 2011
PMID: 21155771
Prey-mediated effects of glucosinolates on aphid predators
PMID: IND44577811
Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators
Chaplin-Kramer R, Kliebenstein DJ, Chiem A, Morrill E, Mills NJ, Kremen C., Journal of applied ecology. 48(4), 2011
PMID: IND44600081
Quantifying predation on folivorous insect larvae: the perspective of life‐history evolution
REMMEL T, DAVISON J, TAMMARU T., Biol J Linn Soc Lond 104(1), 2011
PMID: IND44767847
Folivory versus florivory--adaptiveness of flower feeding.
Bandeili B, Müller C., Naturwissenschaften 97(1), 2010
PMID: 19826770
Activity guided isolation of antioxidants from the leaves of Ricinus communis L
Singh PradeepPratap, Ambika, Chauhan SMS., Food Chem 114(3), 2009
PMID: IND44165733
Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations.
Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA., J Chem Ecol 34(2), 2008
PMID: 18231835
beta-Glucosidases as detonators of plant chemical defense.
Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, Bak S., Phytochemistry 69(9), 2008
PMID: 18472115
The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid
Gols Rieta, Witjes LeontienMA, van Loon JoopJA, Posthumus MaartenA, Dicke Marcel, Harvey JeffreyA., Entomol Exp Appl 128(1), 2008
PMID: IND44067048
Consequences of variation in plant defense for biodiversity at higher trophic levels.
Poelman EH, van Loon JJ, Dicke M., Trends Plant Sci 13(10), 2008
PMID: 18774329
Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae.
Mumm R, Burow M, Bukovinszkine'kiss G, Kazantzidou E, Wittstock U, Dicke M, Gershenzon J., J Chem Ecol 34(10), 2008
PMID: 18787901
Sequestration of furostanol saponins by Monophadnus sawfly larvae.
Prieto JM, Schaffner U, Barker A, Braca A, Siciliano T, Boevé JL., J Chem Ecol 33(3), 2007
PMID: 17252214
Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense.
Harvey JA, Gols R, Wagenaar R, Bezemer TM., J Chem Ecol 33(8), 2007
PMID: 17587139
Biology and biochemistry of glucosinolates.
Halkier BA, Gershenzon J., Annu Rev Plant Biol 57(), 2006
PMID: 16669764
The glucosinolate-myrosinase system in an ecological and evolutionary context.
Kliebenstein DJ, Kroymann J, Mitchell-Olds T., Curr Opin Plant Biol 8(3), 2005
PMID: 15860423
Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae.
Müller C, Wittstock U., Insect Biochem Mol Biol 35(10), 2005
PMID: 16102424
Characterization of the Arabidopsis TU8 glucosinolate mutation, an allele of TERMINAL FLOWER2.
Kim JH, Durrett TP, Last RL, Jander G., Plant Mol Biol 54(5), 2004
PMID: 15356387
Presence of haemocyte-like cells in coccinellid reflex blood.
Karystinou A, Thomas APM, Roy HE., Physiol Entomol 29(1), 2004
PMID: IND43629525
Chemical defence in a sawfly: genetic components of variation in relevant life-history traits.
Müller C, Zwaan BJ, de Vos H, Brakefield PM., Heredity (Edinb) 90(6), 2003
PMID: 12764422
Sequestration of glucosinolates by harlequin bug Murgantia histrionica.
Aliabadi A, Renwick JA, Whitman DW., J Chem Ecol 28(9), 2002
PMID: 12449503

16 References

Daten bereitgestellt von Europe PubMed Central.

Myrosinase: gene family evolution and herbivore defense in Brassicaceae.
Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J., Plant Mol. Biol. 42(1), 2000
PMID: 10688132
1,4-Dimethoxyglucobrassicin in Barbarea and 4-hydroxyglucobrassicin in Arabidopsis and Brassica.
Agerbirk N, Petersen BL, Olsen CE, Halkier BA, Nielsen JK., J. Agric. Food Chem. 49(3), 2001
PMID: 11312886
Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies.
Rodman J, Soltis P, Soltis D, Sytsma K, Karol K., Am. J. Bot. 85(7), 1998
PMID: 21684983
Defensive use by an insect of a plant resin.
Eisner T, Johnessee JS, Carrel J, Hendry LB, Meinwald J., Science 184(4140), 1974
PMID: 4207808
A natural toxic defense system: cardenolides in butterflies versus birds.
Brower LP, Fink LS., Ann. N. Y. Acad. Sci. 443(), 1985
PMID: 3860070
Sequestration of distasteful compounds by some pharmacophagous insects.
Nishida R, Fukami H., J. Chem. Ecol. 16(1), 1990
PMID: 24264904
The chemical diversity and distribution of glucosinolates and isothiocyanates among plants.
Fahey JW, Zalcmann AT, Talalay P., Phytochemistry 56(1), 2001
PMID: 11198818
A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm.
Murray CL, Quaglia M, Arnason JT, Morris CE., J. Neurobiol. 25(1), 1994
PMID: 7906712
Cyanogenesis-a general phenomenon in the lepidoptera?
Witthohn K, Naumann CM., J. Chem. Ecol. 13(8), 1987
PMID: 24302389
Sequestration of phenanthroindolizidine alkaloids by an Asclepiadaceae-feeding danaid butterfly, Ideopsis similis.
Abe F, Yamauchi T, Honda K, Omura H, Hayashi N., Phytochemistry 56(7), 2001
PMID: 11314955


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 11789955
PubMed | Europe PMC

Suchen in

Google Scholar