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Applied Biological Chemistry

, Volume 61, Issue 3, pp 337–343 | Cite as

Effects of Opuntia ficus-indica lectin on feeding, survival, and gut enzymes of maize weevil, Sitophilus zeamais

  • Carolina de Santana Souza
  • Thamara Figueiredo Procópio
  • Bernardo do Rego Belmonte
  • Patrícia Maria Guedes Paiva
  • Lidiane Pereira de Albuquerque
  • Emmanuel Viana Pontual
  • Thiago Henrique Napoleão
Article

Abstract

In this study, the effects of Opuntia ficus-indica lectin (OfiL) on the survival and nutritional parameters of Sitophilus zeamais (maize weevil) adults were evaluated. OfiL was incorporated into the artificial diets at concentrations of 15, 60, and 95 mg/g (mg of lectin per g of wheat flour). Mortality was evaluated after 7 and 15 days, and the amount of food ingested and the weight of the insects were determined on the 7th day. In addition, the in vitro effects of OfiL on the gut enzymes of the insect were investigated. The ingestion of OfiL did not show any significant difference in the mortality rates compared to control. The relative consumption rate was also similar to that of the control, and no deterrent effect was detected. However, the values of the relative biomass variation and the efficiency of ingested food conversion were negative in the treatments at 60 and 95 mg/g, showing that lectin ingestion resulted in weight loss. OfiL exhibited a stimulatory effect on the protease activity from S. zeamais gut extract, which may cause uncontrolled hydrolysis of proteins in the digestive tract. This lectin did not promote significant alteration in the amylase activity. In conclusion, OfiL was able to exert anti-nutritional effects without causing a deterrent effect.

Keywords

Indian-fig Lectin Insecticidal activity Greater rice weevil Agricultural pest 

Notes

Acknowledgments

The authors express their gratitude to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 446902/2014-4; 408789/2016-6) for research grants and fellowship (PMGP). They are also grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; AUXPE 1454/2013) and the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE; APQ-0137-2.08/12; APQ-0108-2.08/14; APQ-0661-2.08/15) for financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Napoleão TH, Agra-Neto AC, Belmonte BR, Pontual EV, Paiva PMG (2015) Biology, ecology and strategies for control of stored-grain beetles: a review. In: Stack C (ed) Beetles: biodiversity, ecology and role in the environment. Nova Science Publishers Inc., New York, pp 105–122Google Scholar
  2. 2.
    Gallo D, Nakano O, Silveira Neto S, Carvalho RPL, Batista GC, Berti Filho E, Parra JRP, Zucchi RA, Alves SB, Vendramim JD, Marchini IC, Lopes JRS, Omoto G (2002) Entomologia Agrícola. FEALQ, PiracicabaGoogle Scholar
  3. 3.
    Botton M, Lorini I, Afonso APS (2005) Ocorrência de Sitophilus zeamais Mots. (Coleoptera: Curculionidae) danificando a cultura da videira no Rio Grande do Sul. Neotrop Entomol 34:355–356CrossRefGoogle Scholar
  4. 4.
    Fazolin M, Costa CR, Damaceno JEO, Albuquerque ES, Cavalcante ASS, Estrela JLV (2010) Fumigação de milho para o controle do gorgulho utilizando caule de Tanaecium nocturnum (Bignoniaceae). Pesq Agropecu Bras 45:1–6CrossRefGoogle Scholar
  5. 5.
    Suleiman RA, Rosentrater KA (2015) Current maize production, postharvest losses and the risk of mycotoxins contamination in Tanzania. In: Agricultural and biosystems engineering conference proceedings and presentations.  https://doi.org/10.13031/aim.20152189434
  6. 6.
    Morales JA, Cardoso DG, Della Lucia TMC, Guedes RNC (2013) Weevil x insecticide: does ‘personality’ matter? PLoS ONE 8:e67283CrossRefGoogle Scholar
  7. 7.
    Beti JA, Philips TW, Smalley EB (1995) Effects of maize weevils (Coleoptera: Curculionidae) on production of aflatoxin B1 by Aspergillus flavus in stored corn. J Econ Entomol 88:1776–1782CrossRefGoogle Scholar
  8. 8.
    Gnonlonfin GJB, Hell K, Adjovi Y, Fandohan P, Koudande DO, Mensah GA, Sanni A, Brimer L (2013) A review on aflatoxin contamination and its implications in the developing world: a sub-Saharan African perspective. Crit Rev Food Sci Nutr 53:349–365CrossRefGoogle Scholar
  9. 9.
    Barra P, Rosso L, Nesci A, Etcheverry M (2013) Isolation and identification of entomopathogenic fungi and their evaluation against Tribolium confusum, Sitophilus zeamais, and Rhyzopertha dominica in stored maize. J Pest Sci 86:217–226CrossRefGoogle Scholar
  10. 10.
    Napoleão TH, Belmonte BR, Pontual EV, Albuquerque LP, Sá RA, Paiva LM, Coelho LCBB, Paiva PMG (2013) Deleterious effects of Myracrodruon urundeuva leaf extract and lectin on the maize weevil, Sitophilus zeamais (Coleoptera, Curculionidae). J Stored Prod Res 54:26–33CrossRefGoogle Scholar
  11. 11.
    Lü J, Zhang H (2016) The effect of acclimation to sublethal temperature on subsequent susceptibility of Sitophilus zeamais Mostchulsky (Coleoptera: Curculionidae) to high temperatures. PLoS ONE 11:e0159400CrossRefGoogle Scholar
  12. 12.
    Camaroti JRSL, Oliveira APS, Paiva PMG, Pontual EV, Napoleão TH (2017) Phytoinsecticides for controlling pests and mosquito vectors of diseases. In: Green V (ed) Biocontrol agents: types, applications and research insights. Nova Science Publishers Inc., New York, pp 147–188Google Scholar
  13. 13.
    Araújo RA, Williamson MS, Bass C, Field LM, Duce IR (2011) Pyrethroid resistance in Sitophilus zeamais is associated with a mutation (T929I) in the voltage gated sodium channel. Insect Mol Biol 20:437–445CrossRefGoogle Scholar
  14. 14.
    Haddi K, Mendonça LP, Santos MF, Guedes RN, Oliveira EE (2015) Metabolic and behavioral mechanisms of indoxacarb resistance in Sitophilus zeamais (Coleoptera: Curculionidae). J Econ Entomol 108:362–369CrossRefGoogle Scholar
  15. 15.
    Freitas RCP, Faroni LRD, Haddi K, Jumbo LOV, Oliveira EE (2016) Allyl isothiocyanate actions on populations of Sitophilus zeamais resistant to phosphine: toxicity, emergence inhibition and repellency. J Stored Prod Res 69:257–264CrossRefGoogle Scholar
  16. 16.
    Cordeiro EMG, Corrêa AS, Denadai CAR, Tomé HVV, Guedes RNC (2017) Insecticide resistance and size assortative mating in females of the maize weevil (Sitophilus zeamais). Pest Manag Sci 73:823–829CrossRefGoogle Scholar
  17. 17.
    Lannoo N, Van Damme EJM (2014) Lectin domains at the frontiers of plant defense. Front Plant Sci 5:397Google Scholar
  18. 18.
    Procópio TF, Moura MC, Albuquerque LP, Gomes FS, Santos NDL, Coelho LCBB, Pontual EV, Napoleão TH (2017) Antibacterial lectins: action mechanisms, defensive roles and biotechnological potential. In: Collins E (ed) Antibacterials: synthesis, properties and biological activities. Nova Science Publishers Inc., New York, pp 69–89Google Scholar
  19. 19.
    Paiva PMG, Pontual EV, Napoleão TH, Coelho LCBB (2013) Lectins and trypsin inhibitors from plants. Biochemical characteristics and adverse effects on insect larvae. Nova Science Publishers Inc., New YorkGoogle Scholar
  20. 20.
    Macedo MLR, Oliveira CFR, Oliveira CT (2015) Insecticidal activity of plant lectins and potential application in crop protection. Molecules 20:2014–2033CrossRefGoogle Scholar
  21. 21.
    Santana GMS, Albuquerque LP, Simões DA, Gusmão NB, Coelho LCBB, Paiva PMG (2009) Isolation of lectin from Opuntia fícus indica cladodes. Acta Hortic 811:281–286CrossRefGoogle Scholar
  22. 22.
    Paiva PMG, Santana GMS, Souza IFAC, Albuquerque LP, Agra-Neto AC, Albuquerque AC, Luz LA, Napoleão TH, Coelho LCBB (2011) Effect of lectins from Opuntia ficus-indica cladodes and Moringa oleifera seeds on survival of Nasutitermes corniger. Int Biodeterior Biodegrad 65:982–989CrossRefGoogle Scholar
  23. 23.
    Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  24. 24.
    Procópio TF, Patriota LLS, Moura MC, Silva PM, Oliveira APS, Carvalho LVN, Lima TA, Coelho LCBB, Soares T, Silva TD, Pitta MGR, Rêgo MJBM, Figueiredo RCBQ, Paiva PMG, Napoleão TH (2017) CasuL: a new lectin isolated from Calliandra surinamensis leaf pinnulae with cytotoxicity to cancer cells, antimicrobial activity and antibiofilm effect. Int J Biol Macromol 98:419–429CrossRefGoogle Scholar
  25. 25.
    Bing DH, Weyand JGM, Stavistsky AB (1967) Hemagglutination with aldehyde-fixed erythrocytes for assay of antigens and antibodies. Proc Soc Exp Biol Med 124:1166–1170CrossRefGoogle Scholar
  26. 26.
    Xie YS, Bodnaryk RP, Fields PG (1996) A rapid and simple flour-disk bioassay for testing substances active against stored-product insects. Can Entomol 28:865–875CrossRefGoogle Scholar
  27. 27.
    Isman MB, Koul O, Luczynski A, Kaminski J (1990) Insecticidal and antifeedant bioactivities of neem oils and their relationship to azadirachtin content. J Agric Food Chem 38:1406–1411CrossRefGoogle Scholar
  28. 28.
    Azeez A, Sane AP, Bhatnagar D, Nath P (2007) Enhanced expression of serine proteases during floral senescence in Gladiolus. Phytochemistry 68:1352–1357CrossRefGoogle Scholar
  29. 29.
    Bernfeld P (1955) Amylases, α and β. Methods Enzymol 1:149–158CrossRefGoogle Scholar
  30. 30.
    Oliveira CFR, Luz LA, Paiva PMG, Coelho LCBB, Marangoni S, Macedo MLR (2011) Evaluation of seed coagulant Moringa oleifera lectin (cMoL) as a bioinsecticidal tool with potential for the control of insects. Process Biochem 46:498–504CrossRefGoogle Scholar
  31. 31.
    Oliveira CFR, Moura MC, Napoleão TH, Paiva PMG, Coelho LCBB, Macedo MLR (2017) A chitin-binding lectin from Moringa oleifera seeds (WSMoL) impairs digestive physiology of the mediterranean flour larvae, Anagasta kuehniella. Pestic Biochem Physiol 142:67–76CrossRefGoogle Scholar
  32. 32.
    Oliveira CT, Kunz D, Silva CP, Macedo MLR (2015) Entomotoxic properties of Dioclea violacea lectin and its effects on digestive enzymes of Anagasta kuehniella (Lepidoptera). J Insect Physiol 81:81–89CrossRefGoogle Scholar
  33. 33.
    Coelho JS, Santos NDL, Napoleão TH, Gomes FS, Ferreira RS, Zingali RB, Coelho LCBB, Navarro DMAF, Paiva PMG (2009) Effect of Moringa oleifera lectin on development and mortality of Aedes aegypti larvae. Chemosphere 77:934–938CrossRefGoogle Scholar
  34. 34.
    Agra-Neto AC, Napoleão TH, Pontual EV, Santos NDL, Luz LA, Oliveira CMF, Melo-Santos MAV, Coelho LCBB, Navarro DMAF, Paiva PMG (2014) Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res 113:175–184CrossRefGoogle Scholar
  35. 35.
    Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29:87–101CrossRefGoogle Scholar
  36. 36.
    Vandenborre G, Smagghe G, Van Damme EJM (2011) Plant lectins as defense proteins against phytophagous insects. Phytochemistry 72:1538–1550CrossRefGoogle Scholar
  37. 37.
    Lima TA, Dornelles LP, Oliveira APS, Guedes CCS, Souza SO, Sá RA, Zingali RB, Napoleão TH, Paiva PMG (2018) Binding targets of termiticidal lectins from the bark and leaf of Myracrodruon urundeuva in the gut of Nasutitermes corniger workers. Pest Manag Sci.  https://doi.org/10.1002/ps.4847 Google Scholar
  38. 38.
    Powell KS, Spence J, Bharathi M, Gatehouse JA, Gatehouse AMR (1998) Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). J Insect Physiol 44:529–539CrossRefGoogle Scholar
  39. 39.
    Lima TA, Fernandes KM, Oliveira APS, Dornelles LP, Martins GF, Napoleão TH, Paiva PMG (2017) Termiticidal lectins from Myracrodruon urundeuva (Anacardiaceae) cause midgut damages when ingested by Nasutitermes corniger (Isoptera; Termitidae) workers. Pest Manag Sci 73:991–998CrossRefGoogle Scholar
  40. 40.
    Li HM, Sun L, Mittapalli O, Muir WM, Xie J, Wu J, Schemerhorn BJ, Sun W, Pittendrigh BR, Murdock LL (2009) Transcriptional signatures in response to wheat germ agglutinin and starvation in Drosophila melanogaster larval midgut. Insect Mol Biol 18:21–31CrossRefGoogle Scholar
  41. 41.
    Pompermayer P, Falco MC, Parra JRP, Silva-Filho MC (2003) Coupling diet quality and Bowman-Birk and Kunitz-type soybean proteinase inhibitor effectiveness to Diatraea saccharalis development and mortality. Entomol Exp Appl 109:217–224CrossRefGoogle Scholar
  42. 42.
    May CM, Doroszuk A, Zwaan BJ (2015) The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster. Ecol Evol 5:1156–1168CrossRefGoogle Scholar
  43. 43.
    Ho SH, Cheng LPL, Sim KY, Tan HTW (1994) Potential of cloves (Syzygium aromaticum (L.) Merr. and Perry) as a grain protectant against Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. Postharvest Biol Technol 4:179–183CrossRefGoogle Scholar

Copyright information

© The Korean Society for Applied Biological Chemistry 2018

Authors and Affiliations

  • Carolina de Santana Souza
    • 1
  • Thamara Figueiredo Procópio
    • 1
  • Bernardo do Rego Belmonte
    • 1
  • Patrícia Maria Guedes Paiva
    • 1
  • Lidiane Pereira de Albuquerque
    • 2
  • Emmanuel Viana Pontual
    • 3
  • Thiago Henrique Napoleão
    • 1
  1. 1.Departamento de Bioquímica, Centro de BiociênciasUniversidade Federal de PernambucoRecifeBrazil
  2. 2.Departamento de Bioquímica e FarmacologiaUniversidade Federal do PiauíTeresinaBrazil
  3. 3.Departamento de Morfologia e Fisiologia AnimalUniversidade Federal Rural de PernambucoRecifeBrazil

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