Interaction between larval α-amylase of the tomato leaf miner, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) and proteinaceous extracts from plant seeds
More details
Hide details
Plant Protection Department, College of Agriculture and Natural Resources, University of Tehran, 31587-77871 Karaj, Iran
Ali Reza Bandani
Plant Protection Department, College of Agriculture and Natural Resources, University of Tehran, 31587-77871 Karaj, Iran
Submission date: 2015-01-12
Acceptance date: 2015-06-17
Journal of Plant Protection Research 2015;55(3):278–286
The tomato leaf miner, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is one of the most destructive pest of solanaceae and it prefers tomato (Solanum lycopersicum L.). The aim of the current study was to investigate the effects of a wide range of seed proteinaceous extracts from different plant families against T. absoluta α-amylase activity. The effect of pH on the inhibitory activity of seed extracts showed that seed extracts of amaranth along with a wheat cultivar (Alvand, Aflak, Sarvdasht, Alborz, and Kavir) produced more than a 50% inhibition of the insect amylase. Aflak wheat seed extract at 10 μg, inhibited 81% of the insect amylase. This percent was the highest inhibition achieved. The other proteinaceous seed extracts had a lower effect on the enzymatic activity. Probit analysis showed that Aflak, Kavir, Alborz, Alvand, Sarvdasht, and amaranth inhibited the amylase activity with an I 50 of 1.94, 3.24, 3.46, 3.31, 4.97, and 15.39 μg, respectively. The effect of pH on the inhibition of the α-amylase showed the highest inhibition of Amaranth and wheat, at a pH value of 8.0, which corresponds to the pH of the insect’s gut. Gel electrophoresis assays confirmed the spectrophotometric assays showing that the α-amylase of the insect gut was affected by the presence of the seed extracts. In the gel assay, a high concentration (14 μg protein) of amaranth proteinaceous seed extract greatly decreased the intensity of the α-amylase band. A high concentration of the Aflak wheat cultivar (10 μg protein) caused the disappearance of the amylase band in the gel. Thus, it is concluded that the physiochemical environment of the insect gut affects the interaction between digestive α-amylase and the metabolites. The experiments showed that seed proteinaceous extracts from non-host plant species, produced more inhibition of the insect amylase when compared to the host plant species. It appears that with evolution, adaptation took place so that insect/s could overcome the plant metabolites.
The authors have declared that no conflict of interests exist.
Baker J. 1987. Purification of isoamylases from the rice weevil Sitophilus oryzae (L.) (Coleoptera: Curculionidae), by highperformance liquid chromatography and their interaction with partially-purified amylase inhibitors from wheat. Insect Biochemistry 17 (1): 37–44.
Bandani A., Amiri B., Butt T.M., Gordon-Weeks R. 2001. Effects of efrapeptin and destruxin, metabolites of entomogenous fungi, on the hydrolytic activity of a vacuolar type ATPase identified on the brush border membrane vesicles of Galleria mellonella midgut and on plant membrane bound hydrolytic enzymes. Biochemica et Biophysica Acta – Biomembranes 1510 (1–2): 367–377.
Bandani A.R., Kazzazi M., Mehrabadi M. 2009. Purification and characterization of midgut α-amylases of Eurygaster integriceps. Entomological Science 12 (1): 25–32.
Bannakan I., Hormchan P., Wongpiyasatid A., Engkakul A. 2007. Effects of α-amylase inhibitor on mungbean weevil, Callosobruchus maculatus, in vivo and in vitro and on barley malt α-amylase in vitro. Kasetsart Journal: Natural Science 41: 451–460.
Barbosa A.E., Albuquerque É.V., Silva M.C., Souza D.S., Oliveira-Neto O.B., Valencia A., Rocha T.L., Grossi-de-Sa M.F. 2010. α-Amylase inhibitor-1 gene from Phaseolus vulgaris expressed in Coffea arabica plants inhibits α-amylases from the coffee berry borer pest. BMC Biotechnology 10 (1): 44.
Berenbaum M. 1980. Adaptive significance of midgut pH in larval Lepidoptera. The American Naturalist 115 (1): 138–146.
Bernfeld P. 1955. Amylases, α and β. Methods in Enzymology 1: 149–154.
Bignell D., Anderson J. 1980. Determination of pH and oxygen status in the guts of lower and higher termites. Journal of Insect Physiology 26 (3): 183–188.
Biondi A., Zappalà L., Stark J.D., Desneux N. 2013. Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLOS ONE 8 (9): e76548. DOI: 10.1371/journal.pone.0076548.
Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1–2): 248–254.
Campolo O., Malacrinò A., Zappalà L., Laudani F., Chiera E., Serra D., Russo M., Palmeri V. 2014. Fumigant bioactivity of five Citrus essential oils against Tribolium confusum. Phytoparasitica 42 (2): 223–233.
Dastranj M., Bandani A.R., Mehrabadi M. 2013. Age-specific digestion of Tenebrio molitor(Coleoptera: Tenebrionidae) and inhibition of proteolytic and amylolytic activity by plant proteinaceous seed extracts. Journal of Asia-Pacific Entomology 16 (3): 309–315.
Desneux N., Wajnberg E., Wyckhuys K.A., Burgio G., Arpaia S., Narváez-Vasquez C.A., González-Cabrera J., Ruescas D.C, Tabone E., Frandon J. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science 83 (3): 197–215.
Desneux N., Luna M.G., Guillemaud T., Urbaneja A. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. Journal of Pest Science 84 (4): 403–408.
Dias S.C., da Silva M.C.M., Teixeira F.R., Figueira E.L.Z., de Oliveira-Neto O.B., de Lima L.A., Franco O.L., Grossi-de Sa M.F. 2010. Investigation of insecticidal activity of rye α-amylase inhibitor gene expressed in transgenic tobacco (Nicotiana tabacum) toward cotton boll weevil (Anthonomus grandis). Pesticide Biochemistry and Physiology 98 (1): 39–44.
Dow J.A.T. 1984. Extremely high pH in biological systems: a model for carbonate transport. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 246: 633–636.
Dow J.A.T. 1986. Insect midgut function. Advanced Insect Physiology 19: 187–328.
Down R.E., Fitches E.C., Wiles D.P., Corti P., Bell H.A., Gatehouse J.A., and Edwards J.P. 2006. Insecticidal spider venom toxin fused to snowdrop lectin is toxic to the peach-potato aphid, Myzus persicae(Hemiptera: Aphididae) and the rice brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Pest Management Science 62 (1): 77–85.
Fitches E., Edwards M.G., Mee C., Grishin E., Gatehouse A.M.R, Edwards J.P., Gatehouse J.A. 2004. Fusion proteins containing insect-specific toxins as pest control agents: snowdrop lectin delivers fused insecticidal spider venom toxin to insect haemolymph following oral ingestion. Journal of Insect Physiology 50 (1): 61–71.
Fitches E.C., Bell H.A., Powell M.E., Back E., Sargiotti C., Weaver R.J., Gatehouse J.A. 2010. Insecticidal activity of scorpion toxin (ButaIT) and snowdrop lectin (GNA) containing fusion proteins towards pest species of different orders. Pest Management Science 66 (1): 74–83.
Franco O.L., Rigden D.J.R., Melo F., Bloch C., Silva C.P., Grossi de Sá M.F. 2000. Activity of wheat α-amylase inhibitors towards bruchid α-amylases and structural explanation of observed specificities. European Journal of Biochemistry 267 (8): 2166–2173.
Franco O.L., Rigden D.J., Melo F.R., Grossie Sá M.F. 2002. Plant α-amylase inhibitors and their interaction with insect α-amylases. European Journal of Biochemistry 269 (2): 397–412.
Gatehouse A.M., Norton E., Davison G.M., Babbé S.M., Newell C.A., Gatehouse J.A. 1999. Digestive proteolytic activity in larvae of tomato moth, Lacanobia oleracea; effects of plant protease inhibitors in vitro and in vivo. Journal of Insect Physiology 45 (6): 545–558.
Guedes R., Picanço M. 2012. The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bulletin 42 (2): 211–216.
Guedes R., Siqueira H. 2013. The tomato borer Tuta absoluta: in-secticide resistance and control failure. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 7 (005): 245.
Harrison R.L., Bonning B.C. 2010. Proteases as insecticidal agents. Toxins 2 (5): 935–953.
Ishimoto M., Sato T., Chrispeels M.J., Kitamura K. 1996. Bruchid resistance of transgenic azuki bean expressing seed α-amylase inhibitor of common bean. Entomologia Experimentalis et Applicata 79 (3): 309–315.
Isman M.B. 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51 (1): 45–66.
Kazzazi M., Bandani A.R., Hosseinkhani S. 2005. Biochemical characterization of α-amylase of the Sunn pest, Eurygaster integriceps. Entomological Science 8 (4): 371–377.
Koiwa H., Bressan R.A., Hasegawa P.M. 1997. Regulation of protease inhibitors and plant defense. Trends in Plant Science 2 (10): 379–384.
Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (5259): 680–685.
Mehrabadi M., Bandani A.R., Saadati F. 2010. Inhibition of Sunn pest, Eurygaster integriceps, α-amylases by α-amylase inhibitors (T-αAI) from Triticale. Journal of Insect Science 10 (179): 1–13.
Mehrabadi M., Bandani A., Saadati F., Mahmudvand M. 2011. α-Amylase activity of stored products insects and its inhibition by medicinal plant extracts. Journal of Agricultural Science & Technology 13: 1173–1182.
Mehrabadi M., Bandani A.R., Mehrabadi R., Alizadeh H. 2012. Inhibitory activity of proteinaceous α-amylase inhibitors from Triticale seeds against Eurygaster integriceps salivary α-amylases: Interaction of the inhibitors and the insect digestive enzymes. Pesticide Biochemistry and Physiology 102 (3): 220–228.
Melo F.R., Sales M.P., Silva L.S., Franco O.L., Bloch J.R.C., Ary M.B. 1999. α-Amylase inhibitors from cowpea seeds. Protein and Peptide Letters 6: 387–392.
Metcalf R.L. 1989. Insect resistance to insecticides. Pesticide Science 26 (4): 333–358.
Payan F. 2004. Structural basis for the inhibition of mammalian and insect α-amylases by plant protein inhibitors. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1696 (2): 171–180.
Reyes M., Rocha K., Alarcón L., Siegwart M., Sauphanor B. 2012. Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta(Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pesticide Biochemistry and Physiology 102 (1): 42–50.
Saadati F., Bandani A.R. 2011. Effects of serine protease inhibitors on growth and development and digestive serine proteinases of the Sunn pest, Eurygaster integriceps. Journal of Insect Science 11 (72): 1–12.
Saadati F., Bandani A.R., Moslemi A. 2011. Effect of plant seeds protein extract on the Sunn pest, Eurygaster integriceps Put on, growth and development and its gut serine protease activity. African Journal of Biotechnology 10: 11502–11510.
SAS Institute 1997. SAS/STAT User’s Guide for Personal Computers. SAS Institute, Cary, Nc.
Savino V., Coviella C.E., Luna M.G. 2012. Reproductive biology and functional response of Dineulophus phtorimaeae, a natural enemy of the tomato moth, Tuta absoluta. Journal of Insect Science 12 (153): 1–14.
Sharma H., Ortiz R. 2000. Transgenics, pest management, and the environment. Current Science 79 (4): 421–437.
Siqueira H., Guedes R., Fragoso D.B., Magalhaes L. 2001. Abamectin resistance and synergism in Brazilian populations of Tuta absoluta(Meyrick) (Lepidoptera: Gelechiidae). International Journal of Pest Management 47 (4): 247–251.
Sivakumar S., Mohan M., Franco O., Thayumanavan B. 2006. Inhibition of insect pest α-amylases by little and finger millet inhibitors. Pesticide Biochemistry and Physiology 85 (3): 155–160.
Svensson B., Fukuda K., Nielsen P.K., Bønsager B.C. 2004. Proteinaceous α-amylase inhibitors. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1696 (2): 145–156.
Rahimi V., Bandani A.R. 2014. Comparison of the effects of cereal and legume proteinaceous seed extracts on α-amylase activity and development of the Sunn pest. Journal of AsiaPacific Entomology 17 (1): 7–11.
Terra W.R., Ferreira C. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 109 (1): 1–62.
Terra W.R., Ferreira C., Baker J.E. 1996. Compartmentalization of digestion. p. 207–235. In: “Biology of the Insect Midgut” (M.J. Lehane, P.F. Billingsley, eds.). Chapman and Hall, London, UK, 486 pp.
Tomé H., Martins J., Corrêa A., Galdino T., Picanço M., Guedes R. 2013. Azadirachtin avoidance by larvae and adult females of the tomato leafminer Tuta absoluta. Crop Protection 46: 63–69.
Tropea Garzia G., Siscaro G., Biondi A., Zappalà L. 2012. Tuta absoluta, a South American pest of tomato now in the EPPO region: biology, distribution and damage. EPPO Bulletin 42 (2): 205–210.
Ussuf K., Laxmi N., Mitra R. 2001. Proteinase inhibitors: plant derived genes of insecticidal protein for developing insectresistant transgenic plants. Current Science-Bangalore 80: 847–853.
Valencia-Jiménez A., Arboleda V.J.W., López-Ávila A.L., Grossi de-Sá M.F. 2008. Digestive α-amylases from Tecia solanivora larvae (Lepidoptera: Gelechiidae): response to pH, temperature and plant amylase inhibitors. Bulletin of Entomological Research 98 (06): 575–579.
Valizadeh B., Zibaee A., Sendi J.J. 2013. Inhibition of digestive α-amylases from Chilo suppressalisWalker (Lepidoptera: Crambidae) by a proteinaceous extract of Citrullus colocynthisL. (Cucurbitaceae). Journal of Plant Protection Research 53 (3): 195–202.
Zappala L., Biondi A., Alma A., Al-Jboory I.J., Arno J., Bayram A., Chailleux A., El-Arnaouty A., Gerling D., Guenaoui Y. 2013. Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. Journal of Pest Science 86 (4): 635–647.
Zappalà L., Siscaro G., Biondi A., Mollá O., González Cabrera J., Urbaneja A. 2012. Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. Journal of Applied Entomology 136 (6): 401–409.
Zibaee A., Bandani A.R., Kafil M., Ramzi S. 2008. Characterization of α-amylase in the midgut and the salivary glands of rice striped stem borer, Chilo suppressalisWalker (Lepidoptera: Pyralidae). Journal of Asia-Pacific Entomology 11 (4): 201–205.