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Insecticidal activity of indole derivatives against Plutella xylostella and selectivity to four non-target organisms

  • Ângela C. F. Costa
  • Sócrates C. H. Cavalcanti
  • Alisson S. Santana
  • Ana P. S. Lima
  • Thaysnara B. Brito
  • Rafael R. B. Oliveira
  • Nathália A. Macêdo
  • Paulo F. Cristaldo
  • Ana Paula A. Araújo
  • Leandro BacciEmail author
Article

Abstract

The diamondback moth Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) is a destructive pest of brassica crops of economic importance that have resistance to a range of insecticides. Indole derivates can exert diverse biological activities, and different effects may be obtained from small differences in their molecular structures. Indole is the parent substance of a large number of synthetic and natural compounds, such as plant and animal hormones. In the present study, we evaluate the insecticidal activity of 20 new synthesized indole derivatives against P. xylostella, and the selectivity of these derivatives against non-target hymenopteran beneficial arthropods: the pollinator Apis mellifera (Linnaeus, 1758) (Hymenoptera: Apidae), and the predators Polybia scutellaris (White, 1841), Polybia sericea (Olivier, 1791) and Polybia rejecta (Fabricius, 1798) (Hymenoptera: Vespidae). Bioassays were performed in the laboratory to determine the lethal and sublethal effects of the compounds on P. xylostella and to examine their selectivity to non-target organisms by topical application and foliar contact. The treatments consisted of two synthesized derivatives (most and least toxic), the positive control (deltamethrin) and the negative control (solvent). The synthesized compound 4e [1-(1H-indol-3-yl)hexan-1-one] showed high toxicity (via topical application and ingestion) and decreased the leaf consumption by P. xylostella, displaying a higher efficiency than the pyrethroid deltamethrin, widely used to control this pest. In addition, the synthesized indole derivatives were selective to the pollinator A. mellifera and the predators P. scutellaris, P. sericea and P. rejecta, none of which were affected by deltamethrin. Our results highlight the promising potential of the synthesized indole derivatives for the generation of new chemical compounds for P. xylostella management.

Keywords

Chemical control Pest control Pesticides Tryptamine 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahuja I, van Dam NM, Winge P et al. (2015) Plant defence responses in oilseed rape mineless plants after attack by the cabbage moth Mamestra brassicae. J Exp Bot 66:579–592.  https://doi.org/10.1093/jxb/eru490 CrossRefGoogle Scholar
  2. Alvarenga E, Carneiro V, Resende G et al. (2012) Synthesis and insecticidal activity of an oxabicyclolactone and novel pyrethroids. Molecules 17:13989–14001.  https://doi.org/10.3390/molecules171213989 CrossRefGoogle Scholar
  3. Bacci L, Picanço MC, da Silva ÉM et al. (2009) Seletividade fisiológica de inseticidas aos inimigos naturais de Plutella xylostella (L.) (Lepidoptera: Plutellidae) em brássicas. Ciênc agrotec (Lavras) 33:2045–2051.  https://doi.org/10.1590/S1413-70542009000700058
  4. Barbosa JD, Silva VB, Alves PB et al. (2012) Structure-activity relationships of eugenol derivatives against Aedes aegypti (Diptera: Culicidae) larvae. Pest Manag Sci 68:1478–1483.  https://doi.org/10.1002/ps.3331 CrossRefGoogle Scholar
  5. Barros EC, Bacci L, Picanco MC et al. (2015) Physiological selectivity and activity reduction of insecticides by rainfall to predatory wasps of Tuta absoluta. J Environ Sci Heal - Part B Pest Food Contam Agric Wastes 50:45–54.  https://doi.org/10.1080/03601234.2015.965621 CrossRefGoogle Scholar
  6. Bortoli SA, Polanczyk R, Vacari A et al. (2013) Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae): tactics for integrated pest management in brassicaceae. In: Soloneski S, Larramendy M (eds) Weed and pest control—conventional and new challenges. InTech, Rijeka, p 31–51Google Scholar
  7. Cerstiaens A, Huybrechts J, Kotanen S et al. (2003) Neurotoxic and neurobehavioral effects of kynurenines in adult insects. Biochem Biophys Res Commun 312:1171–1177.  https://doi.org/10.1016/j.bbrc.2003.11.051 CrossRefGoogle Scholar
  8. Chiou SJ, Kotanen S, Cerstiaens A et al. (1998) Purification of toxic compounds from larvae of the gray fleshfly: the identification of paralysins. Biochem Biophys Res Commun 246:457–462.  https://doi.org/10.1006/bbrc.1998.8644 CrossRefGoogle Scholar
  9. Correa-Cuadros JP, Rodríguez-Bocanegra MX, Sáenz-Aponte A (2014) Susceptibility of Plutella xylostella (Lepidoptera: Plutellidae; Linnaeus 1758) to Beauveria bassiana Bb9205, Metarhizium anisopliae Ma9236 and Heterorhabditis bacteriophora HNI0100. Univ Sci 19:277–285.  https://doi.org/10.11144/Javeriana.SC19-2.spxl Google Scholar
  10. Correia AA, Wanderley-Teixeira V, Teixeira ÁAC et al. (2009) Morfologia do canal alimentar de lagartas de Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae) alimentadas com folhas tratadas com nim. Neotrop Entomol 38:83–91.  https://doi.org/10.1590/S1519-566X2009000100008 CrossRefGoogle Scholar
  11. Du Y, Nomura Y, Zhorov BS, Dong K (2016) Sodium channel mutations and pyrethroid resistance in Aedes aegypti. Insects 7:1–11.  https://doi.org/10.3390/insects7040060 CrossRefGoogle Scholar
  12. Endersby NM, Viduka K, Baxter SW et al. (2011) Widespread pyrethroid resistance in Australian diamondback moth, Plutella xylostella (L.), is related to multiple mutations in the para sodium channel gene. Bull Entomol Res 101:393–405.  https://doi.org/10.1017/S0007485310000684 CrossRefGoogle Scholar
  13. Feng M-L, Li Y-F, Zhu H-J et al. (2012) Design, synthesis, insecticidal activity and structure-activity relationship of 3,3-dichloro-2-propenyloxy-containing phthalic acid diamide structures. Pest Manag Sci 68:986–994.  https://doi.org/10.1002/ps.3243 CrossRefGoogle Scholar
  14. Fernandes ME, de S, Fernandes FL, Picanço MC et al. (2008) Physiological Selectivity of Insecticides to Apis mellifera (Hymenoptera: Apidae) and Protonectarina sylveirae (Hymenoptera: Vespidae) in Citrus. Sociobiology 51:1–10Google Scholar
  15. Gallardo E, Palma-Valdés R, Sarriá B et al. (2016) Synthesis and antioxidant activity of alkyl nitroderivatives of hydroxytyrosol. Molecules 21:656.  https://doi.org/10.3390/molecules21050656 CrossRefGoogle Scholar
  16. Galvan TL, Picanço MC, Bacci L et al. (2002) Seletividade de oito inseticidas a predadores de lagartas em citros. Pesqui Agropecu Bras 37:117–122CrossRefGoogle Scholar
  17. Guirado MM, Elly H, Campos M, De (2009) Alguns aspectos do controle populacional e da resistência a inseticidas em Aedes aegypti (Diptera, Culicidae) Some aspects of the population control and resistance to insecticides in Aedes. Inst Biociências, Let e Ciências Exatas 6:5–14Google Scholar
  18. Han Q, Beerntsen BT, Li J (2007) The tryptophan oxidation pathway in mosquitoes with emphasis on xanthurenic acid biosynthesis. J Insect Physiol 53:254–263.  https://doi.org/10.1016/j.jinsphys.2006.09.004 CrossRefGoogle Scholar
  19. Han Q, Fang J, Li J (2002) 3-hydroxykynurenine transaminase identity with alanine glyoxylate transaminase. J Biol Chem 277:15781–15787.  https://doi.org/10.1074/jbc.M201202200 CrossRefGoogle Scholar
  20. Hasler CM (1998) Functional foods: their role in disease in prevention and health promotion. Food Technol 52:57–62Google Scholar
  21. Higdon JV, Delage B, Williams DE, Dashwood RH (2007) Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharm Res 55:224–236.  https://doi.org/10.1016/j.phrs.2007.01.009 CrossRefGoogle Scholar
  22. Ing HR (1964) The pharmacology of homologous series. In: Progress in drug research, 7th edn. Birkhäuser Basel, Basileia, p 305–339Google Scholar
  23. Kaushik NK, Kushik N, Attri P, Kumar N, Kim CH, Verma AK, Choi EH (2013) Biomedical importance of indoles. Molecules 18:6620–6662.  https://doi.org/10.3390/molecules18066620 CrossRefGoogle Scholar
  24. Lima TC, Santos SRL, Uliana MP et al. (2015) Oxime derivatives with larvicidal activity against Aedes aegypti L. Parasitol Res 114:2883–2891.  https://doi.org/10.1007/s00436-015-4489-9 CrossRefGoogle Scholar
  25. Lin CL, Yeh SC, Feng HT, Dai SM (2017) Inheritance and stability of mevinphos-resistance in Plutella xylostella (L.), with special reference to mutations of acetylcholinesterase 1. Pest Biochem Physiol 141:65–70.  https://doi.org/10.1016/j.pestbp.2016.11.008 CrossRefGoogle Scholar
  26. Nansen C, Baissac O, Nansen M et al. (2016) Behavioral avoidance—will physiological insecticide resistance level of insect strains affect their oviposition and movement responses? PLoS ONE 11:1–12.  https://doi.org/10.1371/journal.pone.0149994 CrossRefGoogle Scholar
  27. Nguyen B, Chompoo J, Tawata S (2015) Insecticidal and nematicidal activities of novel mimosine derivatives. Molecules 20:16741–16756.  https://doi.org/10.3390/molecules200916741 CrossRefGoogle Scholar
  28. Novo MCSS, Prela-Pantano A, Trani PE, Blat SF (2010) Desenvolvimento e produção de genótipos de couve manteiga. Hortic Bras 28:321–325CrossRefGoogle Scholar
  29. Okuda S, Nishiyama N, Saito H, Katsuki H (2002) 3-hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem 70:299–307.  https://doi.org/10.1046/j.1471-4159.1998.70010299.x CrossRefGoogle Scholar
  30. Oliveira RRB, Brito TB, Nepel A et al. (2014) Synthesis, activity, and QSAR studies of tryptamine derivatives on third-instar larvae of Aedes aegypti Linn. Med Chem (Los Angel) 10:580–587Google Scholar
  31. Ottoni O, Neder AVF, Dias AKB et al. (2001) Acylation of indole under Friedel-Crafts conditions-an improved method to obtain 3-acylindoles regioselectively. Org Lett 3:1005–1007.  https://doi.org/10.1021/ol007056i Google Scholar
  32. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353.  https://doi.org/10.1016/j.tree.2010.01.007 CrossRefGoogle Scholar
  33. Raison CG, Standen OD (1955) The schistosomicidal activity of symmetrical diaminodiphenoxyalkanes. Br J Pharm Chemother 10:191–199CrossRefGoogle Scholar
  34. Ramya SL, Venkatesan T, Srinivasa Murthy KS et al. (2016) Detection of carboxylesterase and esterase activity in culturable gut bacterial flora isolated from diamondback moth, Plutella xylostella (Linnaeus), from India and its possible role in indoxacarb degradation. Brazilian. J Microbiol 47:327–336.  https://doi.org/10.1016/j.bjm.2016.01.012 Google Scholar
  35. Ratzka A, Vogel H, Kliebenstein DJ et al. (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci USA 99:11223–11228.  https://doi.org/10.1073/pnas.172112899 CrossRefGoogle Scholar
  36. Rossi F, Garavaglia S, Giovenzana GB et al. (2006) Crystal structure of the Anopheles gambiae 3-hydroxykynurenine transaminase. Proc Natl Acad Sci USA 103:5711–5716.  https://doi.org/10.1073/pnas.0510233103 CrossRefGoogle Scholar
  37. Roszkowski P, Wojtasiewicz K, Leniewski A et al. (2005) Enantioselective synthesis of 1-substituted tetrahydro-β-carboline derivatives via the asymmetric transfer hydrogenation. J Mol Catal A Chem 232:143–149.  https://doi.org/10.1016/j.molcata.2005.01.044 CrossRefGoogle Scholar
  38. Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N (2016) Are bee diseases linked to pesticides? - a brief review. Environ Int 89–90:7–11.  https://doi.org/10.1016/j.envint.2016.01.009 CrossRefGoogle Scholar
  39. Santos LP, Resende JJ, Santos GM, de M et al. (2003) Seletividade de inseticidas a Polybia (Trichothorax) sericea (Oliver, 1791) (Hymenoptera, Vespidae) em condições de laboratório. Rev Bras Zoociências 5:33–44Google Scholar
  40. Santos SRL, Melo MA, Cardoso AV et al. (2011) Structure–activity relationships of larvicidal monoterpenes and derivatives against Aedes aegypti Linn. Chemosphere 84:150–153.  https://doi.org/10.1016/j.chemosphere.2011.02.018 CrossRefGoogle Scholar
  41. SAS Institute (2008). User's Manual, Version 9.2. SAS Institute, Cary, NCGoogle Scholar
  42. Sharma D, Abrol DP (2005) Contact toxicity of some insecticides to honeybee Apis mellifera (L) and Apis cerana (F.). J Asia Pac Entomol 8:113–115.  https://doi.org/10.1016/S1226-8615(08)60079-5 CrossRefGoogle Scholar
  43. Song Z, Chen C-P, Liu J et al. (2016) Design, synthesis, and biological evaluation of (2E)-(2-oxo-1, 2-dihydro-3H-indol-3-ylidene)acetate derivatives as anti-proliferative agents through ROS-induced cell apoptosis. Eur J Med Chem 124:809–819.  https://doi.org/10.1016/j.ejmech.2016.09.005 CrossRefGoogle Scholar
  44. Souza PHM, Souza Neto MH, Maia GA (2003) Componentes funcionais nos alimentos. Bol da SBCTA 37:127–135Google Scholar
  45. Sun J, Zhou Y (2015) Design, synthesis, and insecticidal activity of some novel diacylhydrazine and acylhydrazone derivatives. Molecules 20:5625–5637.  https://doi.org/10.3390/molecules20045625 CrossRefGoogle Scholar
  46. Troczka B, Zimmer CT, Elias J, Schorn C, Bass C, Davies TGE, Field LM, Williamson MS, Slater R, Nauen R (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol Biol 42:873–880.  https://doi.org/10.1016/j.ibmb.2012.09.001 CrossRefGoogle Scholar
  47. Yang J-C, Li M, Wu Q et al. (2016) Design, synthesis and insecticidal evaluation of aryloxy dihalopropene derivatives. Bioorg Med Chem 24:383–390.  https://doi.org/10.1016/j.bmc.2015.09.030 CrossRefGoogle Scholar
  48. Zalucki MP, Shabbir A, Silva R et al. (2012) Estimating the economic cost of one of the world’s major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol 105:1115–1129.  https://doi.org/10.1603/EC12107 CrossRefGoogle Scholar
  49. Zhang C, Qu Y, Wu X et al. (2015) Eco-friendly insecticide discovery via peptidomimetics: design, synthesis, and aphicidal activity of novel insect kinin analogues. J Agric Food Chem 63:4527–4532.  https://doi.org/10.1021/acs.jafc.5b01225 CrossRefGoogle Scholar
  50. Zhou S, Gu Y, Liu M et al. (2014) Insecticidal activities of chiral N-trifluoroacetyl sulfilimines as potential ryanodine receptor modulators. J Agric Food Chem 62:11054–11061.  https://doi.org/10.1021/jf503513n CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ângela C. F. Costa
    • 1
  • Sócrates C. H. Cavalcanti
    • 2
  • Alisson S. Santana
    • 1
  • Ana P. S. Lima
    • 1
  • Thaysnara B. Brito
    • 2
  • Rafael R. B. Oliveira
    • 2
  • Nathália A. Macêdo
    • 2
  • Paulo F. Cristaldo
    • 3
  • Ana Paula A. Araújo
    • 4
  • Leandro Bacci
    • 1
    • 5
    Email author
  1. 1.Programa de Pós-Graduação em Agricultura e BiodiversidadeUniversidade Federal de SergipeSão CristóvãoBrazil
  2. 2.Departamento de FarmáciaUniversidade Federal de SergipeSão CristóvãoBrazil
  3. 3.Programa de Pós-Graduação em Entomologia Agrícola, Departamento de AgronomiaUniversidade Federal Rural de PernambucoRecifeBrazil
  4. 4.Departamento de EcologiaUniversidade Federal de SergipeSão CristóvãoBrazil
  5. 5.Departamento de Engenharia AgronômicaUniversidade Federal de SergipeSão CristóvãoBrazil

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