Skip to main content
SpringerLink
Log in

Glucosinolates on the leaf surface perceived by insect herbivores: review of ambiguous results and new investigations

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Herbivorous insects identify their host plants either by structural features, chemical cues, or a combination. Some insects probe the host leaf prior feeding or oviposition, other species use olfactorial cues or compounds somewhere on the surface. Insects attacking Brassicaceae are no exception, some are attracted and stimulated by volatile isothiocyanates (ITC), many others depend fully on the non-volatile glucosinolates (GS) for host-plant recognition and acceptance. Since most insects have no access to the leaf interior investigators concluded that GS must be present on the leaf surface and ITC in the headspace. However, peelings of mechanically removed surface waxes were devoid of measurable amounts of GS, whereas solvent surface extractions revealed a correlation between stomatal conditions and GS concentrations. Both observations lead to the conclusion that the presence of GS on the top leaf surface is rather unlikely. In the experimental part we show that a chloroform/methanol/water (2:1:1 vol/vol/vol) solvent leaf extract contains GS and, in addition, thia-triaza-fluorenes (TTF), other oviposition stimulants of the cabbage root fly, Delia radicum. Electrophysiological investigations showed that both, GS and TTF stimulated specific receptor neurones of the fly. We suggest that these compounds probably originated from deeper leaf layers and that herbivorous insects may penetrate the wax layer and perceive the stimulating compounds in deeper layers or through the stomata.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

GS:

Glucosinolates

ITC:

Isothiocyanates

TTF:

Thia-triaza-fluorene

References

  • Agerbirk N, De Vos M, Kim JH, Jander G (2008) Indole glucosinolate breakdown and its biological effects. Phytochem Rev (in review)

  • Alborn H, Karlsson H, Lundgren L, Ruuth P, Stenhagen G (1985) Resistance in crop species of the genus Brassica to oviposition by the turnip root fly, Hylemya floralis. Oikos 44(1):61–69. doi:10.2307/3544044

    Article  Google Scholar 

  • Andréasson E, Jørgensen LB (2003) Localization of plant myrosinases and glucosinolates. In: Romeo JT (ed) Recent advances in phytochemistry, vol 37. Pergamon, Amsterdam, pp 79–99

    Google Scholar 

  • Barker AM, Molotsane R, Müller C, Schaffner U, Städler E (2006) Chemosensory and behavioural responses of the turnip sawfly, Athalia rosae, to glucosinolates and isothiocyanates. Chemoecology 16(4):209–218. doi:10.1007/s00049-006-0349-5

    Article  CAS  Google Scholar 

  • Bart KM, Williams EH (1993) Use of dental wax for the study of insect behavior by scanning electron-microscopy. Microsc Res Tech 26(2):180–181. doi:10.1002/jemt.1070260213

    Article  PubMed  CAS  Google Scholar 

  • Baur R, Birch ANE, Hopkins RJ, Griffiths DW, Simmonds MSJ, Städler E (1996) Oviposition and chemosensory stimulation of the root flies Delia radicum and D. floralis in response to plants and leaf surface extracts from resistant and susceptible Brassica genotypes. Entomol Exp Appl 78(1):61–75. doi:10.1007/BF00304457

    Article  Google Scholar 

  • Baur R, Haribal M, Renwick JAA, Städler E (1998) Contact chemoreception related to host selection and oviposition behaviour in the monarch butterfly, Danaus plexippus. Physiol Entomol 23(1):7–19. doi:10.1046/j.1365-3032.1998.2310007.x

    Article  CAS  Google Scholar 

  • Bernays EA, Blaney WM, Chapman RF, Cook AG (1975) The problems of perception of leaf-surface chemicals by locust contact chemoreceptors. In: Denton AD, Coghlan JP (eds) Olfaction and Taste V. Academic, New York, pp 227–229

    Google Scholar 

  • Blaney WM, Simmonds MSJ (1994) Effect of age on the responsiveness of peripheral chemosensory sensilla of the turnip root fly (Delia floralis). Entomol Exp Appl 70(3):253–262. doi:10.1007/BF02380559

    Article  Google Scholar 

  • Blight MM, Pickett JA, Wadhams LJ, Woodcock CM (1995) Antennal perception of oilseed rape, Brassica napus (Brassicaceae), volatiles by the cabbage seed weevil Ceutorhynchus assimilis (Coleoptera: Curculionidae). J Chem Ecol 21(11):1649–1664. doi:10.1007/BF02033667

    Article  CAS  Google Scholar 

  • De Candolle D (1804) Essai sur les propriétés médicales des plantes, comparées avec leurs formes extérieures et leur classification naturelle. L’imprimerie de Didot Jeune de l’imprimeur de l’école de médicine, rue des Macons-Sorbonne, Paris

  • De Jong R, Städler E (1999) The influence of odour on the oviposition behaviour of the cabbage root fly. Chemoecology 9(4):151–154. doi:10.1007/s000490050047

    Article  Google Scholar 

  • De Jong R, Städler E (2001) Sensilla on cabbage root fly tarsae sensitive to egg-associated compounds. Chemoecology 11(3):145–147. doi:10.1007/PL00001844

    Article  Google Scholar 

  • De Jong R, Maher N, Patrian B, Städler E, Winkler T (2000) Rutabaga roots, a rich source of oviposition stimulants for the cabbage root fly. Chemoecology 10(4):205–209. doi:10.1007/PL00001824

    Article  Google Scholar 

  • Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution Int J Org Evolution 8:33–54. doi:10.2307/2405664

    Google Scholar 

  • Dethier VG (1975) The monarch revisited. J Kans Entomol Soc 48(2):129–140

    Google Scholar 

  • De Vos M, Kriksunov K, Jander G (2008) Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae (white cabbage butterfly). Plant Physiol 146(3):916–926. doi:10.1104/pp.107.112185

    Article  PubMed  Google Scholar 

  • Du YJ, van Loon JJA, Renwick JAA (1995) Contact chemoreception of oviposition-stimulating glucosinolates and an oviposition-deterrent cardenolide in 2 subspecies of Pieris napi. Physiol Entomol 20(2):164–174. doi:10.1111/j.1365-3032.1995.tb00813.x

    Article  CAS  Google Scholar 

  • Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194. doi:10.1146/annurev.en.40.010195.001131

    Article  Google Scholar 

  • Eigenbrode SD, Jetter R (2002) Attachment to plant surface waxes by an insect predator. Integr Comp Biol 42(6):1091–1099. doi:10.1093/icb/42.6.1091

    Article  CAS  Google Scholar 

  • Evans KA, Allen-Williams LJ (1992) Electroantennogram responses of the cabbage seed weevil, Ceutorhynchus assimilis, to oilseed rape, Brassica napus ssp oleifera, volatiles. J Chem Ecol 18(9):1641–1659. doi:10.1007/BF00993236

    Article  CAS  Google Scholar 

  • Finch S (1978) Volatile plant-chemicals and their effect on host plant finding by the cabbage root fly (Delia brassicae). Entomol Exp Appl 24(3):350–359. doi:10.1007/BF02385085

    Article  CAS  Google Scholar 

  • Finch S, Skinner G (1982) Trapping cabbage root flies in traps baited with plant extracts and with natural and synthetic isothiocyanates. Entomol Exp Appl 31(2):133–139

    CAS  Google Scholar 

  • Fujikawa K, Seno K, Ozaki M (2006) A novel Takeout-like protein expressed in the taste and olfactory organs of the blowfly, Phormia regina. FEBS J 273(18):4311–4321. doi:10.1111/j.1742-4658.2006.05422.x

    Article  PubMed  CAS  Google Scholar 

  • Gouinguené SPD, Städler E (2005) Comparison of the sensitivity of four Delia species to host and non-host plant compounds. Physiol Entomol 30(1):62–74. doi:10.1111/j.0307-6962.2005.00432.x

    Article  Google Scholar 

  • Gouinguené SPD, Städler E (2006) Comparison of the egg-laying behaviour and electrophysiological responses of Delia radicum and Delia floralis to cabbage leaf compounds. Physiol Entomol 31(4):382–389. doi:10.1111/j.1365-3032.2006.00532.x

    Article  Google Scholar 

  • Griffiths DW, Deighton N, Birch ANE, Patrian B, Baur R, Städler E (2001) Identification of glucosinolates on the leaf surface of plants from the Cruciferae and other closely related species. Phytochem 57(5):693–700. doi:10.1016/S0031-9422(01)00138-8

    Article  CAS  Google Scholar 

  • Holloway PJ, Brown GA, Baker EA, Macey MJK (1977) Chemical composition and ultrastructure of the epicuticular wax in three lines of Brassica napus (L). Chem Phys Lipids 19(2):114–127. doi:10.1016/0009-3084(77)90092-5

    Article  CAS  Google Scholar 

  • Hopkins RJ, Birch ANE, Griffiths DW, Baur R, Städler E, McKinlay RG (1997) Leaf surface compounds and oviposition preference of turnip root fly Delia floralis: the role of glucosinolate and non-glucosinolate compounds. J Chem Ecol 23(3):629–643. doi:10.1023/B:JOEC.0000006400.59702.2f

    Article  CAS  Google Scholar 

  • Hurter J, Ramp T, Patrian B, Städler E, Roessingh P, Baur R et al (1999) Oviposition stimulants for the cabbage root fly: isolation from cabbage leaves. Phytochem 51(3):377–382. doi:10.1016/S0031-9422(99)00062-X

    Article  CAS  Google Scholar 

  • Inoue TA (2006) Morphology of fore-tarsal ventral surfaces of Japanese Papilio butterflies and relations between these morphology, phylogeny and host-plant preferring hierarchy. Zoolog Sci 23(2):169–189. doi:10.2108/zsj.23.169

    Article  PubMed  Google Scholar 

  • Isidoro N, Solinas M, Baur R, Roessingh P, Städler E (1994) Functional morphology of a tarsal sensillum of Delia radicum L. (Diptera: Anthomyiidae) sensitive to important host-plant compounds. Int J Insect Morphol Embryol 23(2):115–125. doi:10.1016/0020-7322(94)90005-1

    Article  Google Scholar 

  • Isidoro N, Bartlet E, Ziesmann J, Williams IH (1998) Antennal contact chemosensilla in Psylliodes chrysocephala responding to cruciferous allelochemicals. Physiol Entomol 23(2):131–138. doi:10.1046/j.1365-3032.1998.232066.x

    Article  Google Scholar 

  • Jeffree CE (1986) The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, functions and evolution. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold, London, pp 23–64

    Google Scholar 

  • Jeffree CE (1996) Structure and ontogeny of plant cuticles. In: Kerstiens G (ed) Plant cuticles. BIOS Scientific Publishers Ltd, Oxford, pp 33–82

    Google Scholar 

  • Juniper BE, Jeffree CE (1983) Plant surfaces. Edward Arnold, London

    Google Scholar 

  • Jørgensen K, Kvello P, Almaas TJ, Mustaparta H (2006) Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens. J Comp Neurol 496(1):121–134. doi:10.1002/cne.20908

    Article  PubMed  Google Scholar 

  • Knoll D, Schreiber L (2000) Plant-microbe interactions: wetting of ivy (Hedera helix L.) leaf surfaces in relation to colonization by epiphytic microorganisms. Microb Ecol 40(1):33–42

    PubMed  Google Scholar 

  • Koch K, Hartmann KD, Schreiber L, Barthlott W, Neinhuis C (2006) Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability. Environ Exp Bot 56(1):1–9. doi:10.1016/j.envexpbot.2004.09.013

    Article  CAS  Google Scholar 

  • Long LM, Patel HP, Cory WC, Stapleton AE (2003) The maize epicuticular wax layer provides UV protection. Funct Plant Biol 30(1):75–81. doi:10.1071/FP02159

    Article  Google Scholar 

  • Ma W-C (1972) Dynamics of feeding responses in Pieris brassicae Linn. as a function of chemosensory input: a behavioural, ultrastructural and electrophysiological study. Meded Landbouwhogeschool Wageningen 72–11:1–162

    Google Scholar 

  • Ma W-C, Schoonhoven LM (1973) Tarsal contact chemosensory hairs of the large white butterfly, Pieris brassicae and their possible rôle in oviposition behaviour. Entomol Exp Appl 16:343–357. doi:10.1007/BF00334245

    Article  Google Scholar 

  • Messchendorp L, Smid HM, van Loon JJA (1998) The role of an epipharyngeal sensillum in the perception of feeding deterrents by Leptinotarsa decemlineata larvae. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 183(2):255–264

    Article  Google Scholar 

  • Miles CI, del Campo ML, Renwick JAA (2005) Behavioral and chemosensory responses to a host recognition cue by larvae of Pieris rapae. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191(2):147–155

    Article  PubMed  Google Scholar 

  • Mitchell BK, Justus KA, Asaoka K (1996) Deterrency and the variable caterpillar: Trichoplusia ni and sinigrin. Entomol Exp Appl 80(1):27–31. doi:10.1007/BF00194717

    Article  CAS  Google Scholar 

  • Müller C (2006) Plant insect interactions on cuticular surfaces. In: Riederer M, Müller C (eds) Biology of the plant cuticle. Annual Plant Reviews, vol 23. Blackwell Publishing, Oxford, pp 398–422

    Chapter  Google Scholar 

  • Müller C (2008) Resistance at the plant cuticle. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, pp 107–129

  • Müller C, Riederer M (2005) Plant surface properties in chemical ecology. J Chem Ecol 31(11):2621–2651. doi:10.1007/s10886-005-7617-7

    Article  PubMed  Google Scholar 

  • Müller C, Agerbirk N, Olsen CE, Boevé JL, Schaffner U, Brakefield PM (2001) Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J Chem Ecol 27(12):2505–2516. doi:10.1023/A:1013631616141

    Article  PubMed  Google Scholar 

  • Nielsen JK (1978) Host plant discrimination within cruciferae—feeding responses of 4 leaf beetles (Coleoptera-Chrysomelidae) to glucosinolates, cucurbitacins and cardenolides. Entomol Exp Appl 24(3):41–54. doi:10.1007/BF00334172

    Article  CAS  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(2):75–83. doi:10.1007/PL00001835

    Article  CAS  Google Scholar 

  • Nottingham SF, Hardie J, Dawson GW, Hick AJ, Pickett JA, Wadhams LJ et al (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. J Chem Ecol 17(6):1231–1242. doi:10.1007/BF01402946

    Article  CAS  Google Scholar 

  • Perleb KJ (1818) Versuch über die Arzneikräfte der Pflanzen verglichen mit den äusseren Formen und der natürlichen Klasseneinteilung derselben (Translation of De Candolle 1804). Sauerländer, Aarau

  • Popp C, Burghardt M, Friedmann A, Riederer M (2005) Characterization of hydrophilic and lipophilic pathways of Hedera helix L. cuticular membranes: permeation of water and uncharged organic compounds. J Exp Bot 56(421):2797–2806. doi:10.1093/jxb/eri272

    Article  PubMed  CAS  Google Scholar 

  • Reifenrath K, Müller C (2008) Multiple feeding stimulants in Sinapis alba for the oligophagous leaf beetle Phaedon cochleariae. Chemoecology 18(1):19–27. doi:10.1007/s00049-007-0389-5

    Article  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(1):41–50. doi:10.1111/j.1570-7458.2005.00242.x

    Article  CAS  Google Scholar 

  • Renwick JAA, Radke CD, Sachdev-Gupta K, Städler E (1992) Leaf surface chemicals stimulating oviposition by Pieris rapae on cabbage. Chemoecology 3(1):33–38. doi:10.1007/BF01261454

    Article  CAS  Google Scholar 

  • Renwick JAA, Haribal M, Gouinguené S, Städler E (2006) Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella. J Chem Ecol 32(4):755–766. doi:10.1007/s10886-006-9036-9

    Article  PubMed  CAS  Google Scholar 

  • Roessingh P, Städler E (1990) Foliar form, color and surface characteristics influence oviposition behavior in the cabbage root fly Delia radicum. Entomol Exp Appl 57(1):93–100. doi:10.1007/BF00349599

    Article  Google Scholar 

  • Roessingh P, Städler E, Schöni R, Feeny P (1991) Tarsal contact chemoreceptors of the black swallowtail butterfly, Papilio polyxenes: responses to phytochemicals from host- and non-host plants. Physiol Entomol 16(4):485–495. doi:10.1111/j.1365-3032.1991.tb00588.x

    Article  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(3):267–282. doi:10.1007/BF02343860

    Article  CAS  Google Scholar 

  • Roessingh P, Städler E, Baur R, Hurter J, Ramp T (1997) Tarsal chemoreceptors and oviposition behaviour of the cabbage root fly (Delia radicum) sensitive to fractions and new compounds of host-leaf surface extracts. Physiol Entomol 22(2):140–148. doi:10.1111/j.1365-3032.1997.tb01151.x

    Article  CAS  Google Scholar 

  • Rohloff J, Bones AM (2005) Volatile profiling of Arabidopsis thaliana—putative olfactory compounds in plant communication. Phytochem 66(16):1941–1955. doi:10.1016/j.phytochem.2005.06.021

    Article  CAS  Google Scholar 

  • Rojas JC (1999) Electrophysiological and behavioral responses of the cabbage moth to plant volatiles. J Chem Ecol 25(8):1867–1883. doi:10.1023/A:1020985917202

    Article  CAS  Google Scholar 

  • Root RB, Kareiva PM (1984) The search for resources by cabbage butterflies (Pieris rapae): ecological consequences and adaptive significance of markovian movements in a patchy environment. Ecology 65:147–165. doi:10.2307/1939467

    Article  Google Scholar 

  • Schoonhoven LM (1967) Chemoreception of mustard oil glucosides in larvae of Pieris brassicae L. Proc K Ned Akad Wet C 5:556–568

    Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Shields VDC, Mitchell BK (1995a) Sinigrin as a feeding deterrent in 2 crucifer-feeding, polyphagous lepidopterous species and the effects of feeding stimulant mixtures on deterrency. Philos Trans R Soc Lond B Biol Sci 347(1322):439–446. doi:10.1098/rstb.1995.0035

    Article  CAS  Google Scholar 

  • Shields VDC, Mitchell BK (1995b) Responses of maxillary styloconic receptors to stimulation by sinigrin, sucrose and inositol in 2 crucifer-feeding, polyphagous lepidopterous species. Philos Trans R Soc Lond B Biol Sci 347(1322):447–457. doi:10.1098/rstb.1995.0036

    Article  CAS  Google Scholar 

  • Shroff R, Vergara F, Muck A, Svatoš A, Gershenzon J (2008) Mass spectrometric imaging of glucosinolates in Arabidopsis thaliana leaves reveals a non-uniform distribution that has significance for plant defense. Proc Natl Acad Sci USA 105(16):6196–6201. doi:10.1073/pnas.0711730105

    Article  PubMed  CAS  Google Scholar 

  • Simmonds MSJ, Blaney WM, Mithen R, Birch ANE, Lewis J (1994) Behavioral and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates. Entomol Exp Appl 71(1):41–57. doi:10.1007/BF02380568

    Article  CAS  Google Scholar 

  • Spencer JL (1996) Waxes enhance Plutella xylostella oviposition in response to sinigrin and cabbage homogenates. Entomol Exp Appl 81(2):165–173. doi:10.1007/BF00192141

    Article  Google Scholar 

  • Spencer JL, Pillai S, Bernays EA (1999) Synergism in the oviposition behavior of Plutella xylostella: sinigrin and wax compounds. J Insect Behav 12(4):483–500. doi:10.1023/A:1020914723562

    Article  Google Scholar 

  • Städler E (2002) Plant chemical cues important for egg deposition by herbivorous insects. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 171–204

    Google Scholar 

  • Städler E, Roessingh P (1991) Perception of surface chemicals by feeding and ovipositing insects. In: Szentesi A, Jermy T (eds) Insect-plants ’89. Symposia Biologica Hungarica, vol 39. Akadémiai Kiadó, Budapest Hungary, pp 71–86

  • Städler E, Schöni R (1990) Oviposition behavior of the cabbage root fly, Delia radicum (L.), influenced by host plant-extracts. J Insect Behav 3(2):195–209. doi:10.1007/BF01417912

    Article  Google Scholar 

  • Städler E, Renwick JAA, Radke CD, Sachdev-Gupta K (1995) Tarsal contact chemoreceptor response to glucosinolates and cardenolides mediating oviposition in Pieris rapae. Physiol Entomol 20(2):175–187. doi:10.1111/j.1365-3032.1995.tb00814.x

    Article  Google Scholar 

  • Städler E, Baur R, de Jong R (2002) Sensory basis of host-plant selection: in search of the “fingerprints” related to oviposition of the cabbage root fly. Acta Zool Acad Sci Hung 48(1):265–280

    Google Scholar 

  • Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J Ecol 92(1):132–141. doi:10.1111/j.1365-2745.2004.00843.x

    Article  Google Scholar 

  • Sutcliffe JF, Mitchell BK (1982) Characterization of galeal sugar and glucosinolate-sensitive cells in Entomoscelis americana adults. J Comp Physiol 146(3):393–399. doi:10.1007/BF00612708

    Article  CAS  Google Scholar 

  • Tanton MT (1977) Response to food plant stimuli by larvae of mustard beetle Phaedon cochleariae. Entomol Exp Appl 22(2):113–122. doi:10.1007/BF00302567

    Article  CAS  Google Scholar 

  • Terofal F (1965) Zum Problem der Wirtsspezifität bei Pieriden (Lep.). Unter besonderer Berücksichtigung der einheimischen Arten Pieris brassicae L., P. napi L. und P. rapae L. Mitt Munch Entomol Ges 55:1–76

    Google Scholar 

  • Thangstad OP, Bones AM, Holton S, Moen L, Rossiter JT (2001) Microautoradiographic localisation of a glucosinolate precursor to specific cells in Brassica napus L. embryos indicates a separate transport pathway into myrosin cells. Planta 213(2):207–213. doi:10.1007/s004250000491

    Article  PubMed  CAS  Google Scholar 

  • Thangstad OP, Gilde B, Chadchawan S, Seem M, Husebye H, Bradley D et al (2004) Cell specific, cross-species expression of myrosinases in Brassica napus, Arabidopsis thaliana and Nicotiana tabacum. Plant Mol Biol 54(4):597–611. doi:10.1023/B:PLAN.0000038272.99590.10

    Article  PubMed  CAS  Google Scholar 

  • Thorsteinson AJ (1953) The chemotactic responses that determine host specificity in an oligophagous insect (Plutella maculipennis Curt.) Lepidoptera). Can J Zool 31:52–72

    Article  CAS  Google Scholar 

  • Tollsten L, Bergström G (1988) Headspace volatiles of whole plants and macerated plant-parts of Brassica and Sinapis. Phytochem 27(7):4013–4018. doi:10.1016/0031-9422(88)83085-1

    Article  CAS  Google Scholar 

  • Van Loon JJA, Blaakmeer A, Griepink FC, van Beek TA, Schoonhoven LM, de Groot A (1992) Leaf surface compound from Brassica oleracea (Cruciferae) induces oviposition by Pieris brassicae (Lepidoptera: Pieridae). Chemoecology 3(1):39–44. doi:10.1007/BF01261455

    Article  Google Scholar 

  • Van Loon JJA, Wang CZ, Nielsen JK, Gols R, Qiu YT (2002) Flavonoids from cabbage are feeding stimulants for diamondback moth larvae additional to glucosinolates: chemoreception and behaviour. Entomol Exp Appl 104(1):27–34. doi:10.1023/A:1021250621756

    Article  Google Scholar 

  • Verschaffelt E (1910) The cause determining the selection of food in some herbivorous insects. Proc K Ned Akad Wet C 13:536–542

    Google Scholar 

  • Wallbank BE, Wheatley GA (1976) Volatile constituents from cauliflower and other crucifers. Phytochem 15(5):763–766. doi:10.1016/S0031-9422(00)94438-8

    Article  CAS  Google Scholar 

  • Wieczorek H (1976) Glycoside receptor of larvae of Mamestra brassicae L (Lepidoptera, Noctuidae). J Comp Physiol 106(2):153–176. doi:10.1007/BF00620496

    Article  CAS  Google Scholar 

  • Zobayed SMA, Armstrong J, Armstrong W (2001) Leaf anatomy of in vitro tobacco and cauliflower plantlets as affected by different types of ventilation. Plant Sci 161(3):537–548. doi:10.1016/S0168-9452(01)00438-1

    Article  CAS  Google Scholar 

  • Zohren E (1968) Laboruntersuchungen zu Massenzucht, Lebensweise, Eiablage und Eiablageverhalten der Kohlfliege, Chortophila brassicae Bouché (Diptera, Anthomyiidae). Z Angew Entomol 62(2):139–188

    Google Scholar 

Download references

Acknowledgements

This project was funded by the Swiss National Science Foundation, grant 31-65016.01 to ES and by the Sonderforschungsbereich 554 of the Deutsche Forschungsgemeinschaft to KR. We thank Andrea Hauser, Thomas Poiger, and Bruno Patrian, Agroscope Changins-Wädenswil at Wädenswil, Switzerland for analysing the TTF of our surface extracts. We appreciate that Caroline Müller and two unknown reviewers discussed and improved the content and Jean Berüter-Cassels clarified and corrected the manuscript.

Author information

Authors and Affiliations

  1. Department of Environmental Sciences, Conservation Biology, University of Basel, St. Johanns-Vorstadt 10, CH-4056, Basel, Switzerland

    Erich Städler

  2. Balmisacher 8, CH-8824, Schönenberg, Switzerland

    Erich Städler

  3. Ecological Field Station Fabrikschleichach, University of Würzburg, Glashüttenstr. 5, D-96181, Rauhenebrach, Germany

    Kerstin Reifenrath

Authors
  1. Erich Städler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kerstin Reifenrath
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erich Städler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Städler, E., Reifenrath, K. Glucosinolates on the leaf surface perceived by insect herbivores: review of ambiguous results and new investigations. Phytochem Rev 8, 207–225 (2009). https://doi.org/10.1007/s11101-008-9108-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-008-9108-2

Keywords

Search

Navigation