Molecular Description of Scorpion Toxin Interaction with Voltage-Gated Sodium Channels

  • Michael Gurevitz
  • Dalia Gordon
  • Maya Gur Barzilai
  • Roy Kahn
  • Lior Cohen
  • Yehu Moran
  • Noam Zilberberg
  • Oren Froy
  • Hagit Altman-Gueta
  • Michael Turkov
  • Ke Dong
  • Izhar Karbat
Living reference work entry


Scorpion alpha and beta toxins interact with voltage-gated sodium channels (Navs) at two pharmacologically distinct sites. Alpha toxins bind at receptor site 3 and inhibit channel inactivation, whereas beta toxins bind at receptor site 4 and shift the voltage-dependent activation toward more hyperpolarizing potentials. The two toxin classes are subdivided to distinct pharmacological groups according to their binding preferences and competition for receptor sites at Nav subtypes. To elucidate the surface of interaction of the two toxin classes with Navs and clarify the molecular basis of varying toxin preferences, an efficient expression system was established. Mutagenesis accompanied by toxicity, binding, and electrophysiological assays, in parallel to determination of the three-dimensional structure using NMR and X-ray crystallography, uncovered the bioactive surfaces of toxin representatives of all pharmacological groups. Exchange of external loops between channels that exhibit marked differences in sensitivity to various toxins accompanied by point mutagenesis highlighted channel determinants that play a role in toxin selectivity. These data were used in further mapping of the brain channel rNav1.2a receptor sites for the beta-toxin Css4 (from Centruroides suffusus suffusus) and the alpha-toxin Lqh2 (from Leiurus quinquestriatus hebraeus). On the basis of channel mutations that affected Css4 activity, the known structure of the toxin and its bioactive surface, and using the structure of a potassium channel as template, a structural model of Css4 interaction with the gating module of domain II was constructed. This initial model was the first step in the identification of part of receptor site 4. In parallel, a swapping and a mutagenesis approach employing the rNav1.2a mammalian and DmNav1 insect Navs and the toxin Lqh2 as a probe were used to search for receptor site 3. The channel mapping along with toxin dissociation assays and double-mutant cycle analyses using toxin and channel mutants identified the gating module of domain IV as the site of interaction with the toxin core domain, thus describing the docking orientation of an alpha toxin at the channel surface.


Receptor Site Scorpion Venom Scorpion Toxin Alpha Toxin Galanthus Nivalis Agglutinin 
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  1. Asamoah OK, Wuskell JP, Loew LM, Bezanilla F. A fluorometric approach to local electric field measurements in a voltage-gated ion channel. Neuron. 2003;37:85–97.PubMedCrossRefGoogle Scholar
  2. Banerjee S, Curto EV, Beckman M, Brown GB, Zhong J, Krishna NR. Expression of functional scorpion neurotoxin Lqq-V in E. coli. Peptides. 2006;27:49–54.PubMedCrossRefGoogle Scholar
  3. Barhanin J, Giglio JR, Léopold P, Schmid A, Sampaio SV, Lazdunski M. Tityus serrulatus venom contains two classes of toxins. J Biol Chem. 1982;257:12553–8.PubMedGoogle Scholar
  4. Ben Khalifa R, Stankiewicz M, Lapied B, Turkov M, Zilberberg N, Gurevitz M, Pelhate M. Refined electrophysiological analysis suggests that a depressant toxin is a sodium channel opener rather than a blocker. Life Sci. 1997;61:819–30.CrossRefGoogle Scholar
  5. Bezanilla F. The voltage sensor in voltage-dependent ion channels. Physiol Rev. 2000;80:555–92.PubMedGoogle Scholar
  6. Bosmans F, Rash L, Zhu S, Diochot S, Lazdunski M, Escoubas P, Tytgat J. Four novel tarantula toxins as selective modulators of voltage-gated sodium channel subtypes. Mol Pharmacol. 2006;69:419–29.PubMedCrossRefGoogle Scholar
  7. Campos FV, Chanda B, Beirão PS, Bezannila F. Alpha-scorpion toxin impairs a conformational change that leads to fast inactivation of muscle sodium channels. J Gen Physiol. 2008;132:251–63.PubMedCentralPubMedCrossRefGoogle Scholar
  8. Catterall WA. Cellular and molecular biology of voltage-gated sodium channels. Physiol Rev. 1992;72:S15–48.PubMedGoogle Scholar
  9. Catterall WA, Cestèle S, Yarov-Yarovoy V, Yu FH, Konoki K, Scheuer T. Voltage-gated ion channels and gating modifier toxins. Toxicon. 2007;49:124–41.PubMedCrossRefGoogle Scholar
  10. Cestèle S, Qu Y, Rogers JC, Rochat H, Catterall WA. Voltage sensor-trapping: enhanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron. 1998;21:919–31.PubMedCrossRefGoogle Scholar
  11. Cestèle S, Scheuer T, Mantegazza M, Rochat H, Catterall WA. Neutralization of gating charges in domain II of the sodium channel a subunit enhances voltage-sensor trapping by a β-scorpion toxin. J Gen Physiol. 2001;118:291–301.PubMedCentralPubMedCrossRefGoogle Scholar
  12. Cestèle S, Yarov-Yarovoy V, Qu Y, Sampieri F, Scheuer T, Catterall WA. Structure and function of the voltage sensor of sodium channels probed by a β-scorpion toxin. J Biol Chem. 2006;281:21332–44.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Chanda B, Asamoah OK, Bezanilla F. Coupling interactions between voltage sensors of the sodium channel as revealed by site-specific measurements. J Gen Physiol. 2004;123:217–30.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cohen L, Karbat I, Gilles N, Froy O, Angelovici R, Gordon D, Gurevitz M. Dissection of the functional surface of an anti-insect excitatory toxin illuminates a putative ‘hot spot’ common to all scorpion β-toxins affecting Na channels. J Biol Chem. 2004;279:8206–11.PubMedCrossRefGoogle Scholar
  15. Cohen L, Karbat I, Gilles N, Ilan N, Gordon D, Gurevitz M. Common features in the functional surface of scorpion β-toxins and elements that confer specificity for insect and mammalian voltage-gated Na-channels. J Biol Chem. 2005;280:5045–53.PubMedCrossRefGoogle Scholar
  16. Cohen L, Lipstein N, Gordon D. Allosteric interactions between scorpion toxin receptor sites on voltage-gated Na channels imply a novel role for weakly active components in arthropod venom. FASEB J. 2006;20:E1360–7.Google Scholar
  17. Cohen L, Ilan N, Gur M, Stühmer S, Gordon D, Gurevitz M. Design of a specific activator for skeletal muscle sodium channels uncovers channel architecture. J Biol Chem. 2007;282:29424–30.PubMedCrossRefGoogle Scholar
  18. Cohen L, Lipstein N, Karbat I, Ilan N, Gilles N, Kahn R, Gordon D, Gurevitz M. Miniaturization of scorpion beta-toxins uncovers a putative ancestral surface of interaction with voltage-gated Na-channels. J Biol Chem. 2008;283:15169–76.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Cory JS. Assessing the risks of releasing genetically modified virus insecticides: progress to date. Crop Prot. 2000;19:779–85.CrossRefGoogle Scholar
  20. Froy O, Gurevitz M. Membrane potential modulators: a thread of scarlet from plants to humans. FASEB J. 1998;12:1793–6.PubMedGoogle Scholar
  21. Froy O, Gurevitz M. New insight on scorpion divergence inferred from comparative analysis of toxin structure, pharmacology and distribution. Toxicon. 2003;42:549–55.PubMedCrossRefGoogle Scholar
  22. Froy O, Zilberberg N, Gordon D, Turkov M, Gilles N, Stankiewicz M, Pelhate M, Loret E, Oren DA, Shaanan B, Gurevitz M. The putative bioactive surface of insect-selective scorpion excitatory neurotoxins. J Biol Chem. 1999;274:5769–76.PubMedCrossRefGoogle Scholar
  23. Gilles N, Krimm I, Bouet F, Froy O, Gurevitz M, Lancelin J-M, Gordon D. Structural implications on the interaction of scorpion α-like toxins with the sodium channel receptor site inferred from toxin iodination and pH-dependent binding. J Neurochem. 2000;75:1735–45.PubMedCrossRefGoogle Scholar
  24. Gordon D. Sodium channels as targets for neurotoxins: mode of action and interaction of neurotoxins with receptor sites on sodium channels. In: Lazarowici P, Gutman Y, editors. Toxins and signal transduction. Amsterdam: Harwood Press; 1997. p. 119–49.Google Scholar
  25. Gordon D, Gurevitz M. The selectivity of scorpion α-toxins for sodium channel subtypes is determined by subtle variations at the interacting surface. Toxicon. 2003;41:125–8.PubMedCrossRefGoogle Scholar
  26. Gordon D, Martin-Eauclaire MF, Cestele S, Kopeyan C, Carlier E, Ben Khalifa R, Pelhate M, Rochat H. Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J Biol Chem. 1996;271:8034–45.PubMedCrossRefGoogle Scholar
  27. Gordon D, Ilan N, Zilberberg N, Gilles N, Urbach D, Cohen L, Karbat I, Froy O, Gaathon A, Kallen RG, Benveniste M, Gurevitz M. An ‘Old World’ scorpion β-toxin that recognizes both insect and mammalian sodium channels: a possible link towards diversification of β-toxins. Eur J Biochem. 2003;270:2663–70.PubMedCrossRefGoogle Scholar
  28. Gordon D, Karbat I, Ilan N, Cohen L, Kahn R, Gilles N, Dong K, Stuhmer W, Tytgat J, Gurevitz M. The differential preference of scorpion alpha-toxins for insect or mammalian sodium channels: implications for improved insect control. Toxicon. 2007;49:452–72.PubMedCrossRefGoogle Scholar
  29. Gur M, Kahn R, Regev-Bar-Ilan N, Wang J, Catterall WA, Gordon D, Gurevitz M. Elucidation of the molecular basis of selective recognition uncovers the interaction site for the core-domain of scorpion alpha-toxins on sodium channels. J Biol Chem. 2011;286:35209–17.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gurevitz M. Mapping the scorpion toxin receptor sites at voltage-gated sodium channels. Toxicon. 2012;60:502–11.PubMedCrossRefGoogle Scholar
  31. Gurevitz M, Zilberberg N. Advances in molecular genetics of scorpion neurotoxins. J Toxicol Toxin Rev. 1994;13:65–100.CrossRefGoogle Scholar
  32. Gurevitz M, Karbat I, Cohen L, Ilan N, Kahn R, Turkov M, Stankiewicz M, Stühmer W, Dong K, Gordon D. The insecticidal potential of scorpion β-toxins. Toxicon. 2007;49:473–89.PubMedCrossRefGoogle Scholar
  33. Heinemann SH, Leipold E. Conotoxins of the O-superfamily affecting voltage-gated sodium channels. Cell Mol Life Sci. 2007;64:1329–40.PubMedCrossRefGoogle Scholar
  34. Herrmann R, Moskowitz H, Zlotkin E, Hammock B. Positive cooperativity among insecticidal scorpion neurotoxins. Toxicon. 1995;33:1099–102.PubMedCrossRefGoogle Scholar
  35. Horn R, Ding S, Gruber HJ. Immobilizing the moving parts of voltage-gated ion channels. J Gen Physiol. 2000;116:461–75.PubMedCentralPubMedCrossRefGoogle Scholar
  36. Jover E, Couraud F, Rochat H. Two types of scorpion neurotoxins characterized by their binding to two separate receptor sites on rat brain synaptosomes. Biochem Biophys Res Commun. 1980;95:1607–14.PubMedCrossRefGoogle Scholar
  37. Kahn R, Karbat I, Ilan N, Cohen L, Gordon D, Gurevitz M. Molecular requirements for specific recognition of brain voltage-gated sodium channels by scorpion alpha-toxins. J Biol Chem. 2009;284:20684–91.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Karbat I, Frolow F, Froy O, Gilles N, Cohen L, Turkov M, Gordon D, Gurevitz M. Molecular basis of the high insecticidal potency of scorpion α-toxins. J Biol Chem. 2004a;279:31679–86.PubMedCrossRefGoogle Scholar
  39. Karbat I, Cohen L, Gilles N, Gordon D, Gurevitz M. Conversion of a scorpion toxin agonist into an antagonist highlights an acidic residue involved in voltage sensor trapping during activation of neuronal Na+ channels. FASEB J. 2004b;18:683–9.PubMedCrossRefGoogle Scholar
  40. Karbat I, Turkov M, Cohen L, Kahn R, Gordon D, Gurevitz M, Frolow F. X-ray structure and mutagenesis of the scorpion depressant toxin LqhIT2 reveals key determinants crucial for activity and anti-insect selectivity. J Mol Biol. 2006;366:586–601.PubMedCrossRefGoogle Scholar
  41. Karbat I, Kahn R, Cohen L, Ilan N, Gilles N, Corzo G, Froy O, Gur M, Albrecht G, Heinemann SH, Gordon D, Gurevitz M. The unique pharmacology of the scorpion α-like toxin Lqh3 is associated with its flexible C-tail. FEBS J. 2007;274:1918–31.PubMedCrossRefGoogle Scholar
  42. Karbat I, Ilan N, Zhang JZ, Cohen L, Kahn R, Benveniste M, Scheuer T, Catterall WA, Gordon D, Gurevitz M. Partial agonist and antagonist activities of a mutant scorpion β-toxin on sodium channels. J Biol Chem. 2010;285:30531–8.PubMedCentralPubMedCrossRefGoogle Scholar
  43. King GF, Escoubas P, Nicholson GM. Peptide toxins that selectively target insect Na(V) and Ca(V). Channels (Austin). 2008;2:100–16.CrossRefGoogle Scholar
  44. Lacroix JJ, Pless SA, Maragliano L, Campos FV, Galpin JD, Ahern CA, Roux B, Bezanilla F. Intermediate state trapping of a voltage sensor. J Gen Physiol. 2012;140:635–52.PubMedCentralPubMedCrossRefGoogle Scholar
  45. Leipold E, Lu S, Gordon D, Hansel A, Heinemann SH. Combinatorial interaction of scorpion toxins Lqh2, Lqh3 and LqhαIT with sodium channel receptor sites-3. Mol Pharmacol. 2004;65:865–91.CrossRefGoogle Scholar
  46. Leipold E, Hansel A, Borges A, Heinemann SH. Subtype specificity of scorpion β-toxin Tz1 interaction with voltage-gated sodium channels is determined by the pore loop of domain-3. Mol Pharmacol. 2006;70:340–7.PubMedGoogle Scholar
  47. Long SB, Campbell EB, MacKinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 2005;309:897–903.PubMedCrossRefGoogle Scholar
  48. Marcotte P, Chen L-Q, Kallen RG, Chahine M. Effects of Tityus serrulatus scorpion toxin γ on voltage-gated Na+ channels. Circ Res. 1997;80:363–9.PubMedCrossRefGoogle Scholar
  49. Martin-Eauclaire MF, Couraud F. Scorpion neurotoxins: effects and mechanisms. In: Chang LW, Dyer RS, editors. Handbook of neurotoxicology. New York: Marcel Dekker; 1995. p. 683–716.Google Scholar
  50. McIntosh M, Cruz LJ, Hunkapiller MW, Gray WR, Olivera BM. Isolation and structure of a peptide toxin from the marine snail Conus magus. Arch Biochem Biophys. 1982;218:329–34.PubMedCrossRefGoogle Scholar
  51. Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao YD, Garsky VM, Bogusky MJ, Mehl JT, Cohen CJ, Smith MM. Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry. 2002;41:14734–47.PubMedCrossRefGoogle Scholar
  52. Miljanich GP. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem. 2004;11:3029–40.PubMedCrossRefGoogle Scholar
  53. Moran Y, Gordon D, Gurevitz M. Sea anemone toxins affecting voltage-gated sodium channels – molecular and evolutionary features. Toxicon. 2009;54:1089–101.PubMedCentralPubMedCrossRefGoogle Scholar
  54. Oren DA, Froy O, Amit E, Kleinberger-Doron N, Gurevitz M, Shaanan B. An excitatory scorpion toxin with a distinctive feature: an additional a-helix at the C-terminus and its implications for interaction with insect sodium channels. Structure. 1998;6:1095–103.PubMedCrossRefGoogle Scholar
  55. Payandeh J, Scheuer T, Zheng N, Catterall WA. The crystal structure of a voltage-gated sodium channel. Nature. 2011;475:353–8.PubMedCentralPubMedCrossRefGoogle Scholar
  56. Pennington MW, Beeton C, Galea CA, Smith BJ, Chi V, Monaghan KP, Garcia A, Rangaraju S, Giuffrida A, Plank D, Crossley G, Nugent D, Khaytin I, Lefievre Y, Peshenko I, Dixon C, Chauhan S, Orzel A, Inoue T, Hu X, Moore RV, Norton RS, Chandy KG. Engineering a stable and selective peptide blocker of the Kv1.3 channel in T lymphocytes. Mol Pharmacol. 2009;75:762–73.PubMedCentralPubMedCrossRefGoogle Scholar
  57. Possani LD, Becerril B, Delepierre M, Tytgat J. Scorpion toxins specific for Na+-channels. Eur J Biochem. 1999;264:287–300.PubMedCrossRefGoogle Scholar
  58. Rash LD, Hodgson WC. Pharmacology and biochemistry of spider venoms. Toxicon. 2002;40:225–54.PubMedCrossRefGoogle Scholar
  59. Rodriguez de la Vega RC, Possani L. Novel paradigms on scorpion toxins that affect the activating mechanism of sodium channels. Toxicon. 2007;49:171–80.CrossRefGoogle Scholar
  60. Rogers JC, Qu Y, Tanada TN, Scheuer T, Catterall WA. Molecular determinants of high affinity binding of α-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the sodium channel α subunit. J Biol Chem. 1996;271:15950–62.PubMedCrossRefGoogle Scholar
  61. Ruta V, Chen J, MacKinnon R. Calibrated measurement of gating-charge arginine displacement in the KvAP voltage-dependent K+ channel. Cell. 2005;123:463–75.PubMedCrossRefGoogle Scholar
  62. Ryan DP, Ptacek LJ. Episodic neurological channelopathies. Neuron. 2010;68:282–92.PubMedCrossRefGoogle Scholar
  63. Shao F, Yu-Mei Xiong Y-M, Zhu R-H, Ling M-H, Chi C-W, Wang D-C. Expression and purification of the BmK M1 neurotoxin from the scorpion Buthus martensii Karsch. Protein Expr Purif. 1999;17:358–65.PubMedCrossRefGoogle Scholar
  64. Smith JJ, Cummins RT, Alphy S, Blumenthal MK. Molecular interactions of the gating modifier toxin, ProTx II, with Nav1.5: implied existence of a novel toxin binding site coupled to activation. J Biol Chem. 2007;282:12687–97.PubMedCrossRefGoogle Scholar
  65. Song W, Du Y, Liu Z, Luo N, Turkov M, Gordon D, Gurevitz M, Goldin AL, Dong K. Mutations in the voltage sensor in domain III enhance the sensitivity of an insect sodium channel to a scorpion β-toxin. J Biol Chem. 2011;286:15781–8.PubMedCentralPubMedCrossRefGoogle Scholar
  66. Strugatsky D, Zilberberg N, Stankiewicz M, Ilan N, Turkov M, Cohen L, Pelhate M, Gilles N, Gordon D, Gurevitz M. Genetic polymorphism and expression of a highly potent scorpion depressant toxin enables refinement of the effects on insect Na-channels and illuminates the key role of Asn-58. Biochemistry. 2005;44:9179–87.PubMedCrossRefGoogle Scholar
  67. Trung N, Fitches E, Gatehouse JA. A fusion protein containing a lepidopteran-specific toxin from the South Indian red scorpion (Mesobuthus tamulus) and snowdrop lectin shows oral toxicity to target insects. BMC Biotechnol. 2006;6:18–30.PubMedCentralCrossRefGoogle Scholar
  68. Tsushima RG, Borges A, Backx PH. Inactivated state dependence of sodium channel modulation by β-scorpion toxin. Eur J Physiol. 1999;437:661–8.CrossRefGoogle Scholar
  69. Turkov M, Rashi S, Zilberberg N, Gordon D, Ben Khalifa R, Stankiewicz M, Pelhate M, Gurevitz M. In vitro folding and functional analysis of an anti-insect selective scorpion depressant neurotoxin produced in E coli. Protein Expr Purif. 1997;9:123–31.CrossRefGoogle Scholar
  70. Villalba-Galea CA, Sandtner W, Dimitrov D, Mutoh H, Knöpfel T, Bezanilla F. Charge movement of a voltage-sensitive fluorescent protein. Biophys J. 2009;96:L19–21.PubMedCentralPubMedCrossRefGoogle Scholar
  71. Wang J, Chen Z, Du J, Sun Y, Lian A. Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Rep. 2005;24:549–55.PubMedCrossRefGoogle Scholar
  72. Wang J, Yarov-Yarovoy V, Kahn R, Gordon D, Gurevitz M, Scheuer T, Catterall WA. Mapping the receptor site for α-scorpion toxins on a Na+ channel voltage sensor. Proc Natl Acad Sci U S A. 2011;108:15426–31.PubMedCentralPubMedCrossRefGoogle Scholar
  73. Weinberger H, Moran Y, Gordon D, Turkov M, Kahn R, Gurevitz M. Positions under positive selection – key for selectivity and potency of scorpion α-toxins. Mol Biol Evol. 2010;27:1025–34.PubMedCrossRefGoogle Scholar
  74. Xiao Y, Bingham JP, Zhu W, Moczydlowski E, Liang S, Cummins TR. Tarantula huwentoxin-IV inhibits neuronal sodium channels by binding to receptor site 4 and trapping the domain II voltage sensor in the closed configuration. J Biol Chem. 2008;283:27300–13.PubMedCentralPubMedCrossRefGoogle Scholar
  75. Yang YC, Kuo CC. The position of the fourth segment of domain 4 determines status of the inactivation gate in Na+ channels. J Neurosci. 2003;23:4922–039.PubMedGoogle Scholar
  76. Ye X, Bosmans F, Li C, Zhang Y, Wang D-C, Tytgat J. Structural basis for the voltage-gated Na channel selectivity of the scorpion a-like toxin BmK M1. J Mol Biol. 2005;353:788–803.PubMedCrossRefGoogle Scholar
  77. Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Jin W, Hasegawa K, Kumasaka T, He J, Jia W, Clapham DE, Yan N. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature. 2012;486:130–4.PubMedCentralPubMedCrossRefGoogle Scholar
  78. Zilberberg N, Froy O, Loret E, Cestèle S, Arad D, Gordon D, Gurevitz M. Identification of structural elements of a scorpion α-neurotoxin important for receptor site recognition. J Biol Chem. 1997;272:14810–6.PubMedCrossRefGoogle Scholar
  79. Zlotkin E. The insect voltage-gated sodium channel as target of insecticides. Annu Rev Entomol. 1999;44:429–55.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Michael Gurevitz
    • 1
  • Dalia Gordon
    • 1
  • Maya Gur Barzilai
    • 1
  • Roy Kahn
    • 1
  • Lior Cohen
    • 2
  • Yehu Moran
    • 3
  • Noam Zilberberg
    • 4
  • Oren Froy
    • 5
  • Hagit Altman-Gueta
    • 1
  • Michael Turkov
    • 1
  • Ke Dong
    • 6
  • Izhar Karbat
    • 1
  1. 1.Department of Plant Molecular Biology & Ecology, George S. Wise Faculty of Life SciencesTel-Aviv UniversityTel-AvivIsrael
  2. 2.Department of Neurobiology, Silberman Institute of Life SciencesHebrew University of JerusalemJerusalemIsrael
  3. 3.Department of Ecology, Evolution and Behavior, Silberman Institute of Life SciencesHebrew University of JerusalemJerusalemIsrael
  4. 4.Department of Life SciencesBen Gurion UniversityBeer ShevaIsrael
  5. 5.Institute of Biochemistry, Food Science and Nutrition, Faculty of AgricultureThe Hebrew University of JerusalemRehovotIsrael
  6. 6.Department of Entomology and the Genetics and Neuroscience ProgramsMichigan State UniversityEast LansingUSA

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