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Non-Volatile Intact Indole Glucosinolates are Host Recognition Cues for Ovipositing Plutella xylostella

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Abstract

The diamondback moth (Plutella xylostella), a crucifer-specialist pest, has been documented to employ glucosinolates as host recognition cues for oviposition. Through the use of mutant Arabidopsis thaliana plants, we investigated the role of specific classes of glucosinolates in the signaling of oviposition by P. xylostella in vivo. Indole glucosinolate production in A. thaliana was found to be crucial in attracting oviposition. Additionally, indole glucosinolates functioned as oviposition cues only when in their intact form. 4-Methoxy-indol-3-ylmethylglucosinolate was implicated as an especially strong oviposition attractant in vitro, suggesting that indole glucosinolate secondary structure may play a role in P. xylostella host recognition as well. Aliphatic glucosinolate-derived breakdown products were found to attract P. xylostella, but only after damage or in the absence of indole glucosinolates. Furthermore, mutant plants lacking both intact indole glucosinolates and aliphatic glucosinolate breakdown products exhibited decreased oviposition attractiveness beyond that of the progenitor mutants lacking either component of the glucosinolate-myrosinase system. Therefore, we conclude that nonvolatile indole glucosinolates and volatile aliphatic glucosinolate breakdown products both appear to play important roles as host recognition cues for P. xylostella oviposition.

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References

  • Barth, C. and Jander, G. 2006. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J. 46:549–562.

    Article  CAS  PubMed  Google Scholar 

  • Baur, R., Haribal, M., Alan, J., Renwick, A., and Städler, E. 1998. Contact chemoreception related to host selection and oviposition behaviour in monarch butterfly, Danaus plexippus. Physiol. Entomol. 23:7–19.

    Article  CAS  Google Scholar 

  • Bednarek, P., Pislewska-Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., Humphry, M., Consonni, C., Panstruga, R., Sanchez-Vallet, A., Molina, A., and Schulze-Lefert, P. 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106.

    Article  CAS  PubMed  Google Scholar 

  • Beekwilder, J., Van Leeuwen, W., Van Dam, N. M., Bertossi, M., Grandi, V., Mizzi, L., Soloview, M., Szabados, L., Molthoff, J. W., Schipper, B., Verbocht, H., De Vos, R. C., Morandini, P., Aarts, M. G., and Bovy, A. 2008. The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS ONE 3:e2068.

  • Brader, G., Tas, É., and Palva, E. T. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant. Physiol. 126:849–860.

    Article  CAS  PubMed  Google Scholar 

  • Choh, Y., Uefune, M., and Takabayashi, J. 2008. Diamondback moth females oviposit more on plants infested by non-parasitised than by parasitised conspecifics. Ecol. Entomol. 33:565–568.

    Article  Google Scholar 

  • Clay, N. K., Adio, A. M., Denoux, C., Jander, G., and Ausubel, F. M. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101.

    Article  CAS  PubMed  Google Scholar 

  • De Vos, M., Kriksunov, K. L., and Jander, G. 2008. Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae (white cabbage butterfly). Plant. Physiol. 146:916–26.

  • De Vos, M. and Jander, G. 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 32:548–560.

  • Gigolashvili, T., Yatusevich, R., Berger, B., Müller, C., and Flügge, U. I. 2007. The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51:247–61.

    Article  CAS  PubMed  Google Scholar 

  • Gigolashvili, T., Engqvist, M., Yatusevich, R., Müller, C., and Flügge, U. I. 2008. HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 177:627.

    Article  CAS  PubMed  Google Scholar 

  • Grubb, C. D. and Abel, S. 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11:89–100.

    Article  CAS  PubMed  Google Scholar 

  • Fahey, J. W., Zalcmann, A. T., and Talalay, P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51.

    Article  CAS  PubMed  Google Scholar 

  • Finch, S. 1978. Volatile plant chemicals and their effect on host plant finding by the cabbage root fly (Delia brassicae). Entomol. Exp. App. 24:350–359.

    Article  CAS  Google Scholar 

  • Furlong, M. J. and Wright, D. J. 1994. Examination of stability of resistance and cross-resistance patterns to acylurea insect growth-regulators in-field populations of the diamondback moth, Plutella xylostella, from Malaysia. Pesticide Sci. 42:315–326.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hansen, B. G., Kliebenstein, D. J., and Halkier, B. A. 2007. Identification of a flavin- monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 50:902–10.

    Article  CAS  PubMed  Google Scholar 

  • Haribal, M. and Renwick, A. 1996. Oviposition stimulants for the monarch butterfly: flavonol glycosides from Asclepias curassavica. Phytochemistry 41:139–144.

    Article  CAS  PubMed  Google Scholar 

  • Heckel, D. G., Gahan, L. J., Liu, Y. B., and Tabashnik, B. E. 1999. Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphasic linkage analysis. Proc. Natl. Acad. Sci. USA 96:8373–8377.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, P. R., Renwick, J. A., and Lopez, K. D. 1997. New oviposition stimulants for the diamondback moth in cabbage. Entomol. Exp. App. 85:281–283.

    Article  CAS  Google Scholar 

  • Iqbal, M. and Wright, D. J. 1997. Evaluation of resistance, cross-resistance and synergism of abamectin and teflubenzuron in a multi-resistant field population of Plutella xylostella (Lepidoptera: Plutellidae). Bull. Entomol. Res. 87:481–486.

    Article  CAS  Google Scholar 

  • Kim, J. H. and 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 

  • Landry, L. G., Chapple C. C. and Last R. L. 1995. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol. 109:1159–1166.

    CAS  Google Scholar 

  • Mumm, R., Bukovinszkine’kiss, G., Kazantzidou, E., Dicke, M., Gershenzon, J. 2008. Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae. J. Chem. Ecol. 34:1311–1321.

    Article  CAS  PubMed  Google Scholar 

  • Pfalz, M., Vogel, H., and Kroymann, J. 2009. The gene controlling the Indole Glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21:985–999.

    Article  CAS  PubMed  Google Scholar 

  • Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T., and Kroymann, J. 2002, Disarming the mustard oil bomb Proc. Natl. Acad. Sci. USA 99:11223–11228.

    Article  CAS  PubMed  Google Scholar 

  • Reed, D. W., Pivnick, K. A., and Underhill, E. W. 1989, Indentification of chemical oviposition stimulants for the diamondback moth, Plutella xylostella, present in three species of Brassicaceae. Entomol. Exp. App. 53:277–286.

    Article  CAS  Google Scholar 

  • Reichelt, M., Brown, P. D., Schneider, B., Oldham, N. J., Stauber, E., Tokuhisa, J., Kliebenstein, D. J., Mitchell-Olds, T. and Gershenzon, J. 2002 Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59:663–671.

    Article  CAS  PubMed  Google Scholar 

  • Renwick, J. A., Haribel, M., Gouinguené, S., and Städler, E. 2006. Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella. J. Chem. Ecol. 32:755–766.

    Article  CAS  PubMed  Google Scholar 

  • Rothschild, M. and Schoonhoven, L. M. 1977. Assessment of egg load by Pieris brassicae (Lepidoptera: Pieridae). Nature 266:352–355.

    Article  Google Scholar 

  • Schroeder, P. C., Shelton, A. M., Ferguson, C. S, Hoffmann, M. P, and Petzoldt, C. H. 2000. Application of synthetic sex pheromone for management of diamondback moth, Plutella xylostella, in cabbage. Entomol. Exp. App. 94:243–248.

    Article  CAS  Google Scholar 

  • Schlaeppi, K., Bodenhausen, N., Buchala, A., Mauch, F., and Reymond, P. 2008. The glutathione-deficient mutant pad2–1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J. 55:774–786.

    Article  CAS  PubMed  Google Scholar 

  • Shroff, R., Vergara, F., Muck, A., Svatoš, A., and Gershenzon, J. 2008. Non-uniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl. Acad. Sci. USA 105:6196–6202.

    Article  CAS  PubMed  Google Scholar 

  • Sønderby, I. E., Hansen, B. G., Bjarnholt, N., Ticconi, C., Halkier, B. A., and Kliebenstein, D. J. 2007. A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2(12):e1322.

    Article  PubMed  Google Scholar 

  • Tabashnik, B. E., Liu, Y. B., Malvar, T., Heckel, D. G., Masson, L., Ballester, V., Granero, F., Mensua, J. L., and Ferre, J. 1997. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 94:12780–12785.

    Article  CAS  PubMed  Google Scholar 

  • Tierens, K. F., Thomma, B. P., Brouwer, M., Schmidt, J., Kistner, K., Porzel, A., Mauch-Mani, B., Cammue, B. P., Broekaert, W. F. (2001). Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol. 125:1688–1699.

    Article  CAS  PubMed  Google Scholar 

  • Tollsten, L. and Bergström , G. 1988. Headspace volatiles of whole plants and macerated plant parts of Brassica and Sinapis. Phytochemistry 27:2073–2077.

    Article  CAS  Google Scholar 

  • Zhao, Y., Hull, A. K., Gupta, N. R., Goss, K. A., Alonso, J., Ecker, J. R., Normanly, J., Chory, J., and Celenza, J. L. 2002. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev. 16:3100–12.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Adewale Martins Adio for the isolation of intact indole glucosinolates. This research was supported by NSF grant IOS-0718733 to GJ and funding from Faculty of Life Sciences, University of Copenhagen to IES.

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Authors and Affiliations

  1. Boyce Thompson Institute for Plant Biology, 1 Tower Rd, Ithaca, NY, 14853, USA

    Joel Y. Sun, Georg Jander & Martin de Vos

  2. Department of Plant Biology and Biotechnology, VKR Research Centre for Pro-Active Plants, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark

    Ida E. Sønderby & Barbara A. Halkier

Authors
  1. Joel Y. Sun
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  2. Ida E. Sønderby
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  3. Barbara A. Halkier
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  4. Georg Jander
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  5. Martin de Vos
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Correspondence to Martin de Vos.

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Figure S1

Chromatograms showing the desulphoglucosinolate profiles of Col-0 and cyp79B2 cyp79B3 (B2B3) chloroform extracts. Indole glucosinolates were identified based on the absorption profiles (229 nm) and retention time in comparison to purified standards. I3M = indol-3-ylmethyl, 4M-I3M = 4-methoxy-indol-3-ylmethyl, 1M-I3M = 1-methoxy-indol-3-ylmethyl. (PPT 152 kb)

Table S1

Foliar glucosinolate content of Col-0 wild-type and glucosinolate-myrosinase system knockout mutants. Significance determined by two-tailed unpaired Student’s t-tests. *P < 0.05, **P < 0.01, ***P < 0.001. Glucosinolate side chain abbreviations are: 3MSP = 3-methylsulfinylpropyl, 4MSB = 4-methylsulfinylbutyl, 5MSP = 5-methylsulfinylpentyl, 4OH-I3M = 4-hydroxy-indol-3-ylmethyl, 7MSH = 7-methylsulfinylheptyl, 4MTB = 4-methylthiobutyl, 8MSO = 8-methylsulfinyloctyl, I3M = indol-3-ylmethyl, 4M-I3M = 4-methoxy-indol-3-ylmethyl, 1M-I3M = 1-methoxy-indol-3-ylmethyl. (PPT 93 kb)

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Sun, J.Y., Sønderby, I.E., Halkier, B.A. et al. Non-Volatile Intact Indole Glucosinolates are Host Recognition Cues for Ovipositing Plutella xylostella . J Chem Ecol 35, 1427–1436 (2009). https://doi.org/10.1007/s10886-009-9723-4

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