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Interactions between glucosinolate- and myrosinase-containing plants and the sawfly Athalia rosae

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Abstract

Several insects have specialised on using Brassicaceae as host plants. Therefore, they evolved metabolic pathways to cope with the defensive glucosinolate–myrosinase system of their diet. Larvae of the turnip sawfly, Athalia rosae L. (Hymenoptera: Tenthredinidae), incorporate various glucosinolates from their hosts into their haemolymph. The ability to sequester these metabolites makes A. rosae a useful model system to study mechanisms of glucosinolate metabolism in this species compared to other specialists, and to study effects of sawfly feeding on levels of glucosinolates and their hydrolysing enzymes in plants. The levels of plant metabolites might in turn directly affect the performance of the insect. On the one hand, costs for glucosinolate uptake and avoidance of myrosinase activity were postulated. On the other hand, sequestration of glucosinolates can be part of the insect’s defence against several predators. Here, the findings on glucosinolate metabolic pathways are compared between different herbivores and the sawfly. The impact of different glucosinolate levels and myrosinase activities on the performance of A. rosae is discussed. Furthermore, effects of feeding by A. rosae larvae on the chemical composition and enzyme activities of various Brassicaceae species are summarised. Induction patterns vary not only between different plant species and cultivars but also due to the inducing agent. Finally, the plant–herbivore interactions are discussed with regard to the sawflies’ defence abilities against different carnivore guilds.

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References

  • Agerbirk N, Müller C, Olsen CE, Chew FS (2006) A common pathway for detoxification of 4-hydroxybenzylglucosinolate in Pieris and Anthocaris (Lepidoptera: Pieridae). Biochem Syst Ecol 34:189–198. doi:10.1016/j.bse.2005.09.005

    Article  CAS  Google Scholar 

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500. doi:10.1034/j.1600-0706.2000.890308.x

    Article  Google Scholar 

  • Agrawal AA, Kurashige NS (2003) A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol 29:1403–1415. doi:10.1023/A:1024265420375

    Article  PubMed  CAS  Google Scholar 

  • Aliabadi A, Renwick JAA, Whitman DW (2002) Sequestration of glucosinolates by Harlequin bug Murgantia histrionica. J Chem Ecol 28:1749–1762. doi:10.1023/A:1020505016637

    Article  PubMed  CAS  Google Scholar 

  • Andréasson E, Jørgensen LB (2003) Localization of plant myrosinases and glucosinolates. In: Romeo JT (ed) Recent advances in phytochemistry. Pergamon, Amsterdam, pp 79–99

    Google Scholar 

  • Andréasson E, Wretblad S, Granér G, Wu X, Zhang J, Dixelius C et al (2001) The myrosinase-glucosinolate system in the interaction between Leptosphaeria maculans and Brassica napus. Mol Plant Pathol 2:281–286. doi:10.1046/j.1464-6722.2001.00076.x

    Article  Google Scholar 

  • Arand K (2006) Spezifität der Glucosinolatsequestration bei Athalia spp. und deren ökologische Relevanz. Diploma Thesis, University of Würzburg, Germany

  • Bartlet E, Blight MM, Lane P, Williams IH (1997) The responses of the cabbage seed weevil Ceutorhynchus assimilis to volatile compounds from oilseed rape in a linear track olfactometer. Entomol Exp Appl 85:257–262. doi:10.1023/A:1003140219888

    Article  Google Scholar 

  • Bartlet E, Kiddle G, Williams I, Wallsgrove R (1999) Wound-induced increases in the glucosinolate content of oilseed rape and their effect on subsequent herbivory by a crucifer specialist. Entomol Exp Appl 91:163–167. doi:10.1023/A:1003661626234

    Article  CAS  Google Scholar 

  • Bede JC, Musser RO, Felton GW, Korth KL (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. doi:10.1007/s11103-005-4923-y

    Article  PubMed  CAS  Google Scholar 

  • Blande JD, Pickett JA, Poppy GM (2007) A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae. J Chem Ecol 33:767–779. doi:10.1007/s10886-007-9264-7

    Article  PubMed  CAS  Google Scholar 

  • Bodnaryk RP (1992) Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard. Phytochemistry 31:2671–2677. doi:10.1016/0031-9422(92)83609-3

    Article  CAS  Google Scholar 

  • Boevé J-L, Müller C (2005) Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators. Chemoecology 15:51–58. doi:10.1007/s00049-005-0292-x

    Article  CAS  Google Scholar 

  • Boevé J-L, Schaffner U (2003) Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134:104–111. doi:10.1007/s00442-002-1092-4

    Article  PubMed  Google Scholar 

  • Bones AM, Rossiter JT (1995) Glucosinolates in cruciferous crops. In: Scarisbrick DH, Ferguson AJ (eds) New horizons in oilseed rape. Semundo, Cambridge, pp 46–67

    Google Scholar 

  • Bradburne RP, Mithen R (2000) Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica. Proc R Soc Lond B Biol Sci 267:89–95. doi:10.1098/rspb.2000.0971

    Article  CAS  Google Scholar 

  • Bridges M, Jones AME, Bones AM, Hodgson C, Cole R, Bartlet E et al (2002) Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc R Soc Lond B Biol Sci 269:187–191. doi:10.1098/rspb.2001.1861

    Article  CAS  Google Scholar 

  • Chew FS (1988) Biological effects of glucosinolates. In: Cutler HG (ed) Biologically active natural products—potential use in agriculture. American Chemical Society Symposium, Washington, DC, pp 155–181

    Google Scholar 

  • Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653. doi:10.1111/j.1365-294X.2004.02161.x

    Article  PubMed  CAS  Google Scholar 

  • de Cock R, Matthysen E (2001) Do glow-worm larvae (Coleoptera: Lampyridae) use warning coloration? Ethology 107:1019–1033. doi:10.1046/j.1439-0310.2001.00746.x

    Article  Google Scholar 

  • de Vos M, van Oosten VR, van Poecke RMP, van Pelt JA, Pozo MJ, Mueller MJ et al (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:932–937. doi:10.1094/MPMI-18-0923

    Google Scholar 

  • Desneux N, Fauvergue X, Dechaume-Moncharmont FX, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J Econ Entomol 98:9–17

    Article  PubMed  Google Scholar 

  • Dicke M, Hilker M (2003) Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl Ecol 4:3–14. doi:10.1078/1439-1791-00129

    Article  CAS  Google Scholar 

  • Doughty KJ, Blight MM, Bock CH, Fieldsend JK, Pickett JA (1996) Release of alkenyl isothiocyanates and other volatiles from Brassica rapa seedlings during infection by Alternaria brassicae. Phytochemistry 43:371–374. doi:10.1016/0031-9422(96)00189-6

    Article  CAS  Google Scholar 

  • ElSayed G, Louveaux A, Mavratzotis M, Rollin P, Quinsac A (1996) Effects of glucobrassicin, epiprogoitrin and related breakdown products on locusts feeding: Schouwia purpurea and desert locust relationships. Entomol Exp Appl 78:231–236. doi:10.1007/BF00187521

    Article  CAS  Google Scholar 

  • Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51. doi:10.1016/S0031-9422(00)00316-2

    Article  PubMed  CAS  Google Scholar 

  • Falk KL, Gershenzon J (2007) The desert locust, Schistocerca gregaria, detoxifies the glucosinolates of Schouwia purpurea by desulfation. J Chem Ecol 33:1542–1555. doi:10.1007/s10886-007-9331-0

    Article  PubMed  CAS  Google Scholar 

  • Feeny P (1977) Defensive ecology of the Cruciferae. Ann Mo Bot Gard 64:221–234. doi:10.2307/2395334

    Article  Google Scholar 

  • Fleishman LJ (1992) The influence of the sensory system and the environment on motion patterns in the visual-displays of Anoline lizards and other vertebrates. Am Nat 139:S36–S61. doi:10.1086/285304

    Article  Google Scholar 

  • Gigolashvili T, Berger B, Mock H-P, Müller C, Weisshaar B, Flügge U-I (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901. doi:10.1111/j.1365-313X.2007.03099.x

    Article  PubMed  CAS  Google Scholar 

  • Gols R, Harvey JA (2008) Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids. Phytochem Rev (this issue). doi:10.1007/s11101-008-9104-6

  • Goodman D (1971) Differential selection of immobile prey among terrestrial and riparian lizards. Am Midl Nat 86:217–219. doi:10.2307/2423704

    Article  Google Scholar 

  • Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100. doi:10.1016/j.tplants.2005.12.006

    Article  PubMed  CAS  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333. doi:10.1146/annurev.arplant.57.032905.105228

    Article  PubMed  CAS  Google Scholar 

  • Heads PA, Lawton JH (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation. Ecol Entomol 10:29–42. doi:10.1111/j.1365-2311.1985.tb00532.x

    Article  Google Scholar 

  • Hilker M, Daloze D, Pasteels JM (1992) Cardenolide glycosides from the adults and eggs of Chrysolina fuliginosa (Coleoptera, Chrysomelidae). Experientia 48:1023–1027. doi:10.1007/BF01919158

    Article  CAS  Google Scholar 

  • Hilker M, Stein C, Schröder R, Varama M, Mumm R (2005) Insect egg deposition induces defence responses in Pinus sylvestris: characterisation of the elicitor. J Exp Biol 208:1849–1854. doi:10.1242/jeb.01578

    Article  PubMed  Google Scholar 

  • Hoffstadt M (2006) Der Einfluss von Glucosinolaten auf die Physiologie von Athalia spp. Diploma Thesis, Universität Würzburg, Germany

  • Howe HF, Westley LC (1993) Anpassung und Ausbeutung – Wechselbeziehungen zwischen Pflanzen und Tieren. Spektrum Akademischer, Verlag, Heidelberg

    Google Scholar 

  • Husebye A, Arzt S, Burmeister WP, Härtel FV, Brandt A, Rossiter JT et al (2004) Crystal structure at 1.1 Å resolution of an insect myrosinase from Brevicoryne brassicae shows its close relationship to ß-glucosidases. Insect Biochem Mol Biol 35:1311–1320. doi:10.1016/j.ibmb.2005.07.004

    Article  CAS  Google Scholar 

  • Jones AME, Bridges M, Bones AM, Cole R, Rossiter JT (2001) Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). Insect Biochem Mol Biol 31:1–5. doi:10.1016/S0965-1748(00)00157-0

    Article  PubMed  CAS  Google Scholar 

  • Jones AME, Winge P, Bones AM, Cole R, Rossiter JT (2002) Characterization and evolution of a myrosinase from the cabbage aphid Brevicoryne brassicae. Insect Biochem Mol Biol 32:275–284. doi:10.1016/S0965-1748(01)00088-1

    Article  PubMed  CAS  Google Scholar 

  • Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA, Bones AM et al (2007) The cabbage aphid: a walking mustard oil bomb. Proc R Soc Lond B Biol Sci 274:2271–2277. doi:10.1098/rspb.2007.0237

    Article  CAS  Google Scholar 

  • Kiddle GA, Doughty KJ, Wallsgrove RM (1994) Salicylic acid-induced accumulation of glucosinolates in oilseed rape (Brassica napus L.) leaves. J Exp Bot 45:1343–1346. doi:10.1093/jxb/45.9.1343

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Koritsas VM, Lewis JA, Fenwick GR (1991) Glucosinolate responses of oilseed rape, mustard and kale to mechanical wounding and infestation by cabbage stem flea beetle (Psylliodes chrysocephala). Ann Appl Biol 118:209–222. doi:10.1111/j.1744-7348.1991.tb06099.x

    Article  Google Scholar 

  • Kuśnierczyk A (2008) Arabidopsis thaliana responses to aphid infestation. PhD Thesis, Norwegian University of Science and Technology, Norway

  • Lee JM, Hashino Y, Hatakeyama M, Oishi K, Naito T (1998) Egg deposition behavior in the haplodiploid sawfly Athalia rosae ruficornis Jakovlev (Hymenoptera: Symphyta: Tenthredinidae). J Insect Behav 11:419–428. doi:10.1023/A:1020958831972

    Article  Google Scholar 

  • Li Q, Eigenbrode SD, Stringham GR, Thiagarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419. doi:10.1023/A:1005535129399

    Article  CAS  Google Scholar 

  • Ludwig-Müller J, Schubert B, Pieper K, Ihmig S, Hilgenberg W (1997) Glucosinolate content in susceptible and resistant Chinese cabbage varieties during development of clubroot disease. Phytochemistry 44:407–417. doi:10.1016/S0031-9422(96)00498-0

    Article  Google Scholar 

  • Ludwig-Müller J, Bennett RN, Kiddle G, Ihmig S, Ruppel M, Hilgenberg W (1999) The host range of Plasmodiophora brassicae and its relationship to endogenous glucosinolate content. New Phytol 141:443–458. doi:10.1046/j.1469-8137.1999.00368.x

    Article  Google Scholar 

  • Ludwig-Müller J, Bennett RN, Garcia-Garrido JM, Piche Y, Vierheilig H (2002) Reduced arbuscular mycorrhizal root colonization in Tropaeolum majus and Carica papaya after jasmonic acid application can not be attributed to increased glucosinolate levels. J Plant Physiol 159:517–523. doi:10.1078/0176-1617-00731

    Article  Google Scholar 

  • MacGibbon DB, Beuzenberg EJ (1978) Location of glucosinolase in Brevicoryne brassicae and Lipaphis erysimi (Aphididae). N Z J Sci 21:389–392

    CAS  Google Scholar 

  • Marples NM, Vanweelen W, Brakefield PM (1994) The relative importance of color, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim Behav 48:967–974. doi:10.1006/anbe.1994.1322

    Article  Google Scholar 

  • Martin N, Müller C (2007) Induction of plant responses by a sequestering insect: relationship of glucosinolate concentration and myrosinase activity. Basic Appl Ecol 8:13–25. doi:10.1016/j.baae.2006.02.001

    Article  CAS  Google Scholar 

  • Matile P (1980) The mustard oil bomb—compartmentation of the myrosinase system. Biochem Physiol Pflanz 175:722–731

    CAS  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435. doi:10.1007/s004250050210

    Article  CAS  Google Scholar 

  • Memmott J, Godfray HCJ, Bolton B (1993) Predation and parasitism in a tropical herbivore community. Ecol Entomol 18:348–352. doi:10.1111/j.1365-2311.1993.tb01111.x

    Article  Google Scholar 

  • Ménard R, Larue J-P, Silué D, Thouvenot D (1999) Glucosinolates in cauliflower as biochemical markers for resistance against downy mildew. Phytochemistry 52:29–35. doi:10.1016/S0031-9422(99)00165-X

    Article  Google Scholar 

  • Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162. doi:10.1104/pp.104.053389

    Article  PubMed  CAS  Google Scholar 

  • Mewis I, Tokuhisa J, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67:2450–2462. doi:10.1016/j.phytochem.2006.09.004

    Article  PubMed  CAS  Google Scholar 

  • Mithöfer A, Wanner G, 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. doi:10.1104/pp.104.054460

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Arand K (2007) Trade-offs in oviposition choice? Food-dependent performance and defence against predators of a herbivorous sawfly. Entomol Exp Appl 124:153–159. doi:10.1111/j.1570-7458.2007.00558.x

    Article  Google Scholar 

  • Müller C, Brakefield PM (2003) Analysis of a chemical defense in sawfly larvae: easy bleeding targets predatory wasps in late summer. J Chem Ecol 29:2683–2694. doi:10.1023/B:JOEC.0000008012.73092.01

    Article  PubMed  Google Scholar 

  • Müller C, Riederer M (2005) Review: plant surface properties in chemical ecology. J Chem Ecol 31:2621–2651. doi:10.1007/s10886-005-7617-7

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Sieling N (2006) Effects of glucosinolate and myrosinase levels in Brassica juncea on a glucosinolate-sequestering herbivore—and vice versa. Chemoecology 16:191–201. doi:10.1007/s00049-006-0347-7

    Article  CAS  Google Scholar 

  • Müller C, Wittstock U (2005) Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae. Insect Biochem Mol Biol 35:1189–1198. doi:10.1016/j.ibmb.2005.06.001

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Agerbirk N, Olsen CE, Boevé J-L, Schaffner U, Brakefield PM (2001) Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J Chem Ecol 27:2505–2516. doi:10.1023/A:1013631616141

    Article  PubMed  Google Scholar 

  • Müller C, Boevé J-L, Brakefield PM (2002) Host plant derived feeding deterrence towards ants in the turnip sawfly Athalia rosae. Entomol Exp Appl 104:153–157. doi:10.1023/A:1021202929313

    Article  Google Scholar 

  • Müller C, Agerbirk N, Olsen CE (2003) Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13:47–54. doi:10.1007/s000490300005

    Article  Google Scholar 

  • Newman RM, Hanscom Z, Kerfoot WC (1992) The watercress glucosinolate-myrosinase system: a feeding deterrent to caddisflies, snails and amphipods. Oecologia 92:1–7. doi:10.1007/BF00317255

    Article  Google Scholar 

  • Nielsen JK, Dalgaard L, Larsen LM, Sorensen H (1979) Host plant selection of the horseradish flea beetle Phyllotreta armoraciae (Coleoptera: Chrysomelidae): feeding response to glucosinolates from several crucifers. Entomol Exp Appl 25:227–239. doi:10.1007/BF00302784

    Article  Google Scholar 

  • Nielsen JK, Hansen ML, Agerbirk N, Petersen BL, Halkier BA (2001) Responses of the flea beetles Phyllotreta nemorum and P. cruciferae to metabolically engineered Arabidopsis thaliana with an altered glucosinolate profile. Chemoecology 11:75–83. doi:10.1007/PL00001835

    Article  CAS  Google Scholar 

  • Ohara Y, Nagasaki K, Ohsaki N (1993) Warning coloration in sawfly Athalia rosae larva and concealing coloration in butterfly Pieris rapae larva on similar plants evolved through individual selection. Res Popul Ecol 19:223–230. doi:10.1007/BF02513594

    Article  Google Scholar 

  • Pasteels JM, Daloze D, Rowell-Rahier M (1986) Chemical defense in chrysomelid eggs and neonate larvae. Physiol Entomol 11:29–37. doi:10.1111/j.1365-3032.1986.tb00388.x

    Article  CAS  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. doi:10.1046/j.1570-7458.2003.00088.x

    Article  Google Scholar 

  • Pontoppidan B, Hopkins R, Rask L, 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. doi:10.1016/j.plantsci.2004.10.003

    Article  CAS  Google Scholar 

  • Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci USA 99:11223–11228. doi:10.1073/pnas.172112899

    Article  PubMed  CAS  Google Scholar 

  • Rayor LS (2004) Effects of monarch larval host plant chemistry and body size on Polistes wasp predation. In: Oberhauser KS, Solensky MJ (eds) The Monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 39–46

    Google Scholar 

  • Reifenrath K, Müller C (2007) Species-specific and leaf-age dependent effects of ultraviolet radiation on two Brassicaceae. Phytochemistry 68:875–885. doi:10.1016/j.phytochem.2006.12.008

    Article  PubMed  CAS  Google Scholar 

  • Reifenrath K, Riederer M, Müller C (2005) Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae. Entomol Exp Appl 115:41–50. doi:10.1111/j.1570-7458.2005.00242.x

    Article  CAS  Google Scholar 

  • Renwick JAA (2002) The chemical world of crucivores: lures, treats and traps. Entomol Exp Appl 104:35–42. doi:10.1023/A:1021231732022

    Article  CAS  Google Scholar 

  • Renwick JAA, Lopez K (1999) Experience-based food consumption by larvae of Pieris rapae: addiction to glucosinolates? Entomol Exp Appl 91:51–58. doi:10.1023/A:1003693005761

    Article  CAS  Google Scholar 

  • Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147. doi:10.1105/tpc.104.026120

    Article  PubMed  CAS  Google Scholar 

  • Roessingh P, Städler E, Fenwick GR, Lewis JA, Nielsen JK, Hurter J et al (1992) Oviposition and tarsal chemoreceptors of the cabbage root fly are stimulated by glucosinolates and host plant-extracts. Entomol Exp Appl 65:267–282. doi:10.1007/BF02343860

    Article  CAS  Google Scholar 

  • Rossiter JT, Jones AM, Bones AM (2003) A novel myrosinase-glucosinolate defense system in Cruciferous specialist aphids. In: Romeo JT (eds) Integrative phytochemistry: from ethnobotany to molecular ecology. Pergamon, Amsterdam. Recent Adv Phytochem 37: 127–142

  • Schaffner U, Boevé J-L, Gfeller H, Schlunegger UP (1994) Sequestration of Veratrum alkaloids by specialist Rhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) and its ecoethological implications. J Chem Ecol 20:3233–3250. doi:10.1007/BF02033723

    Article  CAS  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2006) Insect-plant biology. Oxford University Press, Oxford

    Google Scholar 

  • Seifert B (1996) Ameisen beobachten bestimmen. Naturbuch Verlag, Augsburg

    Google Scholar 

  • Shattuck VI (1993) Glucosinolates and glucosinolate degradation in seeds from turnip mosaic-virus-infected rapid cycle Brassica campestris L. plants. J Exp Bot 44:963–970. doi:10.1093/jxb/44.5.963

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Sillman AJ (1973) Avial vision. In: Farner DS, King JR, Parkes KC (eds) Avial biology. Academic Press, New York, pp 349–387

    Google Scholar 

  • Städler E, Reifenrath K (2008) Insect herbivores perceiving glucosinolates on the leaf surface? Phytochem Rev (this issue). doi:10.1007/s11101-008-9108-2

  • Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A et al (2000) Induced plant defense responses against chewing insects. Ethylen signaling reduces resistance of Arabidopsis against Egyptian Cotton Worm but not Diamondback Moth. Plant Physiol 124:1007–1017. doi:10.1104/pp.124.3.1007

    Article  PubMed  CAS  Google Scholar 

  • Tanton MT (1977) Response to food plant stimuli by larvae of the mustard beetle Phaedon cochleariae. Entomol Exp Appl 22:113–122. doi:10.1007/BF00302567

    Article  CAS  Google Scholar 

  • Textor S, Gershenzon J (2008) Herbivore induction of the glucosinolate-myrosinase defense system: Major trends, biochemical basis and ecological significance. Phytochem Rev (this issue). doi:10.1007/s11101-008-9117-1

  • Travers-Martin N, Müller C (2007) Specificity of induction responses in a Brassicaceae and their effects on a specialist herbivore. J Chem Ecol 33:1582–1597

    Article  PubMed  CAS  Google Scholar 

  • Travers-Martin N, Müller C (2008) Specificity of induction responses in Sinapis alba L.: plant growth and development. Plant Signal Behav 3:311–313

    PubMed  Google Scholar 

  • Traw MB (2002) Is induction response negatively correlated with constitutive resistance in black mustard? Evolution 56:2196–2205

    PubMed  Google Scholar 

  • Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532. doi:10.1007/s00442-002-0924-6

    Article  Google Scholar 

  • Tumlinson JH, Lait CG (2005) Biosynthesis of fatty acid amide elicitors of plant volatiles by insect herbivores. Arch Insect Biochem Physiol 58:54–68. doi:10.1002/arch.20036

    Article  PubMed  CAS  Google Scholar 

  • van Dam NM, Raaijmakers CE (2006) Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and B. oleracea. Chemoecology 16:17–24. doi:10.1007/s00049-005-0323-7

    Article  CAS  Google Scholar 

  • van Dam NM, Harvey JA, Wäckers FL, Bezemer TM, van der Putten WH, Vet LEM (2003) Interactions between aboveground and belowground induced responses against phytophages. Basic Appl Ecol 4:63–77. doi:10.1078/1439-1791-00133

    Article  Google Scholar 

  • van Loon JJA, Frentz WH, Vaneeuwijk FA (1992) Electroantennogram responses to plant volatiles in 2 species of Pieris butterflies. Entomol Exp Appl 62:253–260. doi:10.1007/BF00353444

    Article  Google Scholar 

  • Vergara F, Svatos A, Schneider B, Reichelt M, Gershenzon J, Wittstock U (2006) Glycine conjugates in a lepidopteran insect herbivore—the metabolism of benzylglucosinolate in the cabbage white butterfly, Pieris rapae. Chembiochem 7:1982–1989. doi:10.1002/cbic.200600280

    Article  PubMed  CAS  Google Scholar 

  • Verschaffelt E (1910) The cause determining the selection of food in some herbivorous insects. Proc Acad Sci Amst 13:536–542

    Google Scholar 

  • Vlieger L, Brakefield PM, Müller C (2004) Effectiveness of the defence mechanism of the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae), against predation by lizards. Bull Entomol Res 94:283–289. doi:10.1079/BER2004299

    Article  PubMed  CAS  Google Scholar 

  • von Dahl CC, Hävecker M, Schlögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant–herbivore interactions? Plant J 46:948–960. doi:10.1111/j.1365-313X.2006.02760.x

    Article  CAS  Google Scholar 

  • Wallace SK, Eigenbrode SD (2002) Changes in the glucosinolate-myrosinase defense system in Brassica juncea cotyledons during seedling development. J Chem Ecol 28:243–256. doi:10.1023/A:1017973005994

    Article  PubMed  CAS  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Weber G, Oswald S, Zöllner U (1986) Die Wirtseignung von Rapssorten unterschiedlichen Glucosinolatgehaltes für Brevicoryne brassicae (L.) und Myzus persicae (Sulzer) (Hemiptera, Aphididae). Z Pflanzenkr Pflanzenschutz 93:113–124

    CAS  Google Scholar 

  • Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270. doi:10.1016/S1360-1385(02)02273-2

    Article  PubMed  CAS  Google Scholar 

  • Wittstock U, Kliebenstein DJ, Lambrix V, Reichelt M, Gershenzon J (2003) Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. In: Romeo JT (ed) Recent advances in phytochemistry. Pergamon, Amsterdam, pp 101–125

    Google Scholar 

  • Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T et al (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci USA 101:4859–4864. doi:10.1073/pnas.0308007101

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The author is grateful to Katja Arand, Melanie Hoffstadt and Nora Travers-Martin who worked on different projects with Athalia rosae and to Jean-Luc Boevé who introduced her to the fascinating phenomenon of ‘easy bleeding’ in sawflies. Much of the work was supported by the European Community’s Improving Human Potential Programme under contract HPRN-CT-1999-00054, INCHECO and by the Sonderforschungsbereich 567 “Interspezifische Interaktionen” of the Deutsche Forschungsgemeinschaft.

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Müller, C. Interactions between glucosinolate- and myrosinase-containing plants and the sawfly Athalia rosae . Phytochem Rev 8, 121–134 (2009). https://doi.org/10.1007/s11101-008-9115-3

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