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Glucosinolate Desulfation by the Phloem-Feeding Insect Bemisia tabaci

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Abstract

Glucosinolates are plant secondary defense metabolites confined nearly exclusively to the order Brassicales. Upon tissue rupture, glucosinolates are hydrolyzed to various bioactive breakdown products by the endogenous plant enzyme myrosinase. As the feeding of chewing insect herbivores is associated with plant tissue damage, these insects have developed several independent strategies for coping with the glucosinolate-myrosinase defense system. On the other hand, our knowledge of how phloem-feeding insects interact with the glucosinolate-myrosinase system is much more limited. In fact, phloem feeders might avoid contact with myrosinase altogether so their susceptibility to intoxication by glucosinolate hydrolysis products is unclear. Previous studies utilizing Arabidopsis thaliana plants accumulating high levels of aliphatic- or indolic-glucosinolates indicated that both glucosinolate groups have moderate negative effects on the reproductive performance of Bemisia tabaci, a generalist phloem-feeding insect. To get a deeper understanding of the interaction between B. tabaci and glucosinolate-defended plants, adults were allowed to feed on artificial diet containing intact glucosinolates or on Brussels sprout and A. thaliana plants, and their honeydew was analyzed for the presence of possible metabolites. We found that B. tabaci is capable of cleaving off the sulfate group of intact glucosinolates, producing desulfoglucosinolates that cannot be activated by myrosinases, a mechanism described to date only in several chewing insect herbivores. The presence of desulfated glucosinolates in the honeydew of a generalist phloem-feeder may indicate the necessity to detoxify glucosinolates, likely due to some level of cellular damage during feeding, which results in glucosinolate activation, or as a mechanism to circumvent the non-enzymatic breakdown of indolic glucosinolates.

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References

  • Agerbirk N, De Vos M, Kim JH, Jander G (2009) Indole glucosinolate breakdown and its biological effects. Phytochem Rev 8:101–120

    Article  CAS  Google Scholar 

  • Barth C, 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 

  • Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481

    Article  CAS  PubMed  Google Scholar 

  • De Vos M, Van Oosten VR, Van Poecke RMP et al (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937

    Article  PubMed  Google Scholar 

  • Elbaz M, Halon E, Malka O et al (2012) Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Mol Ecol 21:4533–4546

    Article  CAS  PubMed  Google Scholar 

  • Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol Plant Microbe Interact 27:747–756

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Verrall SR, Hancock RD (2014) Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects. J Exp Bot 66:495–512

    Article  PubMed  Google Scholar 

  • Frerigmann H, Böttcher C, Baatout D, Gigolashvili T (2012) Glucosinolates are produced in trichomes of Arabidopsis thaliana. Front Plant Sci 3:1–13

    Article  Google Scholar 

  • Graser G, Schneider B, Oldham NJ, Gershenzon J (2000) The methionine chain elongation pathway in the biosynthesis of glucosinolates in Eruca sativa (Brassicaceae). Arch Biochem Biophys 378:411–419

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heaney RK, Fenwick GR (1980) Glucosinolates in Brassica vegetables. Analysis of 22 varieties. J Sci Food Agric 31:785–793

    Article  CAS  Google Scholar 

  • Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521

    Article  CAS  PubMed  Google Scholar 

  • Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865

    Article  CAS  PubMed  PubMed Central  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 

  • Koroleva OA, Cramer R (2011) Single-cell proteomic analysis of glucosinolate-rich S-cells in Arabidopsis thaliana. Methods 54:413–423

    Article  CAS  PubMed  Google Scholar 

  • Koroleva OA, Gibson TM, Cramer R, Stain C (2010) Glucosinolate-accumulating S-cells in Arabidopsis leves and flower stalks undergo programmed cell death at early stages of differentiation. Plant J 64:456–469

    Article  CAS  PubMed  Google Scholar 

  • Markovich O, Kafle D, Elbaz M et al (2013) Arabidopsis thaliana plants with different levels of aliphatic- and indolyl-glucosinolates affect host selection and performance of Bemisia tabaci. J Chem Ecol 39:1361–1372

    Article  CAS  PubMed  Google Scholar 

  • Mikkelsen MD, Hansen CH, Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275:33712–33717

    Article  CAS  PubMed  Google Scholar 

  • Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R et al (2009) Disruption of adenosine-59-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21:910–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Opitz SEW, Mix A, Winde IB, Müller C (2011) Desulfation followed by sulfation: metabolism of benzylglucosinolate in Athalia rosae (Hymenoptera: Tenthredinidae). ChemBioChem 12:1252–1257

    Article  CAS  PubMed  Google Scholar 

  • Pentzold S, Zagrobelny M, Rook F, Bak S (2014) How insects overcome two-component plant chemical defence: plant β-glucosidases as the main target for herbivore adaptation. Biol Rev 89:531–551

    Article  PubMed  Google Scholar 

  • Ratzka A, Vogel H, Kliebenstein DJ et al (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci U S A 99:11223–11228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarsby J, Towers MW, Stain C et al (2012) Mass spectrometry imaging of glucosinolates in Arabidopsis flowers and siliques. Phytochemistry 77:110–118

    Article  CAS  PubMed  Google Scholar 

  • Schramm K, Vassão DG, Reichelt M et al (2012) Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Mol Biol 42:174–182

    Article  CAS  PubMed  Google Scholar 

  • Shroff R, Schramm K, Jeschke V et al (2015) Quantification of plant surface metabolites by matrix-assisted laser desorption-ionization mass spectrometry imaging: glucosinolates on Arabidopsis thaliana leaves. Plant J 81:961–972

    Article  CAS  PubMed  Google Scholar 

  • Textor S, Gershenzon J (2009) Herbivore induction of the glucosinolate-myrosinase defense system: major trends, biochemical bases and ecological significance. Phytochem Rev 8:149–170

    Article  CAS  Google Scholar 

  • Van de Ven WT, LeVesque CS, Perring TM, Walling LL (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–1423

    Article  PubMed  PubMed Central  Google Scholar 

  • Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–66

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye XD, Su YL, Zhao QY, Xia WQ, Liu SS et al (2014) Transcriptomic analyses reveal the adaptive features and biological differences of guts from two invasive whitefly species. BMC Genomics 15:370

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Israel Science Foundation grant 1039/12 and by the Max Planck Society. We acknowledge the late Prof. Shalom W. Applebaum for generously supporting our early LCMS analyses by Dr. Julius Ben-Ari at the Interdepartmental Equipment Unit of the Faculty of Agriculture, Food and Environment.

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Authors and Affiliations

  1. Department of Entomology, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Osnat Malka & Shai Morin

  2. Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany

    Anton Shekhov, Michael Reichelt, Jonathan Gershenzon & Daniel Giddings Vassão

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  1. Osnat Malka
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  2. Anton Shekhov
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  3. Michael Reichelt
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  4. Jonathan Gershenzon
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  5. Daniel Giddings Vassão
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  6. Shai Morin
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Correspondence to Osnat Malka.

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Malka, O., Shekhov, A., Reichelt, M. et al. Glucosinolate Desulfation by the Phloem-Feeding Insect Bemisia tabaci . J Chem Ecol 42, 230–235 (2016). https://doi.org/10.1007/s10886-016-0675-1

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  • DOI: https://doi.org/10.1007/s10886-016-0675-1

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