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Change in malate dehydrogenase and alpha amylase activities in Rubus fruticosus and Valeriana jatamansi treated granary weevil, Sitophilus granarius

Mudança nas atividades de malato desidrogenase e alfa amilase em Rubus fruticosus e gorgulho tratado com Valeriana jatamansi, Sitophilus granarius

Abstract

Poor storage conditions provide favorable environment to stored grain pests for their growth. The bio-pesticides are the best alternatives to synthetic pesticides. Present study was conducted to compare toxicity of Rubus fruticosus and Valeriana jatamansi against granary weevil, Sitophilus granarius and subsequent changes in enzyme activity responsible for grain damage. In current research 5 g of R. fruticosus fruit and V. jatamansi rhizome powders were tested separately against S. granarius, in 50 g wheat whole grains for seven days in comparison with the control. The enzymatic activity of malate dehydrogenase and α-amylase was observed in the cellular extracts of S. granarius. The insects were crushed and homogenized in phosphate-buffer solution and centrifuged at 10000 rpm for 5 minutes. For the enzymatic measurement supernatant was tested; the spectrophotometer was adjusted at 340 nm. The reagents were mixed and incubated at 25 °C for five minutes. The cuvettes were placed in the experimental and reference sites of spectrophotometer and recorded the change in absorbance for 3-4 minutes. There was 5.60% and 14.92% reduction in the activity of malate dehydrogenase in R. fruticosus and V. jatamansi, treated insects, respectively. The alpha amylase enzyme activity was 6.82% reduced and 63.63% increase in R. fruticosus and V. jatamansi, treated insects, respectively. Present study addresses that both plant powders are effective against granary weevil by altering enzyme activities so both the plant powders can be used as bio-pesticides against the stored grains pests.

Keywords:
granary weevil; pests; biopesticides; malate dehydrogenase; α-amylase

Resumo

As más condições de armazenamento proporcionam um ambiente favorável às pragas armazenadas para o crescimento. Os biopesticidas são as melhores alternativas aos pesticidas sintéticos. O presente estudo foi conduzido para comparar a toxicidade de Rubus fruticosus e Valeriana jatamansi contra gorgulhos, Sitophilus granarius e subsequentes alterações na atividade enzimática responsáveis ​​por danos aos grãos. Na pesquisa atual, 5 g de frutos de R. fruticosus e pós de rizoma de V. jatamansi foram testados separadamente contra S. granarius, em 50 g de grãos integrais de trigo por sete dias, em comparação com o controle. A atividade enzimática da malato desidrogenase e α-amilase foi observada nos extratos celulares de S. granarius. Os insetos foram esmagados e homogeneizados em solução tampão fosfato e centrifugados a 10000 rpm por 5 minutos. Para a medição enzimática, o sobrenadante foi testado; o espectrofotômetro foi ajustado a 340 nm. Os reagentes foram misturados e incubados a 25 °C por cinco minutos. As cubetas foram colocadas nos locais experimentais e de referência do espectrofotômetro e registradas as alterações na absorbância por 3-4 minutos. Houve redução de 5,60% e 14,92% na atividade da malato desidrogenase em R. fruticosus e V. jatamansi, insetos tratados, respectivamente. A atividade da enzima alfa amilase foi reduzida em 6,82% e aumento de 63,63% em R. fruticosus e V. jatamansi, insetos tratados, respectivamente. O presente estudo aborda que ambos os pós de plantas são eficazes contra o gorgulho do celeiro, alterando as atividades enzimáticas, de modo que ambos os pós de plantas possam ser usados ​​como biopesticidas contra pragas de grãos armazenados.

Palavras-chave:
gorgulho; pragas; biopesticidas; malato desidrogenase; α-amilase

1. Introduction

Cereals are main source of human diet with production exceeding 2100 million tons annually (Shewry, 2007SHEWRY, P.R., 2007. Improving the protein content and composition of cereal grain. Journal of Cereal Science, vol. 46, no. 3, pp. 239-250. http://dx.doi.org/10.1016/j.jcs.2007.06.006.
http://dx.doi.org/10.1016/j.jcs.2007.06....
). Bulk of harvested crop (50%) is lost during storage (Fornal et al., 2007FORNAL, J., JELIŃSKI, T., SADOWSKA, J., GRUNDAS, S., NAWROT, J., NIEWIADA, A., WARCHALEWSKI, J.R. and BŁASZCZAK, W., 2007. Detection of grainer yweevil Sitophilus granarius L., eggs and internal stage analysis. Journal of Stored Products Research, vol. 43, no. 2, pp. 142-148. http://dx.doi.org/10.1016/j.jspr.2006.02.003.
http://dx.doi.org/10.1016/j.jspr.2006.02...
). The poor storage conditions provide favorable environment for the growth of stored grain pests (Stoll, 2000STOLL, G., 2000. Natural crop protection in the tropics, letting information comes on life: Agrecol/CTA. 2nd ed. Weikersheim: Magraf, pp. 23-89.). Insect pests of cereals are responsible for reduction in quantity and quality of food grains (Udo, 2011UDO, I.O., 2011. Potentials of Zanthoxylum xanthoxyloides (LAM.) for the control of stored product insect pests. Journal of Stored Products and Postharvest Research, vol. 2, no. 3, pp. 40-44.). The weight losses in stored products are mainly associated with activities of insect pests (Arlian, 2002ARLIAN, L.G., 2002. Arthropod allergens and human health. Annual Review of Entomology, vol. 47, no. 1, pp. 395-433. http://dx.doi.org/10.1146/annurev.ento.47.091201.145224. PMid:11729080.
http://dx.doi.org/10.1146/annurev.ento.4...
). According to an estimate, annual yield losses due to insect pest are 20-40 percent in overall agricultural products (FAO, 2018FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS – FAO, 2018 [viewed 15 Jan 2012]. Codexalimentarius [online]. Rome: FAO. Available from: https://www.fao.org/fao-who-codexalimentarius/en/Pesticides
https://www.fao.org/fao-who-codexaliment...
). About 1000 insect pests have been reported in harvested products worldwide (Atwal and Dhaliwal, 2008ATWAL, A.S. and DHALIWAL, G.S., 2008. Agricultural pests of South Asia and their management. New Delhi: Kalyani Publishers.). Many strategies have been adopted to preserve cereals from pest infestations; including pesticides, bio pesticides, repellants, fumigants and biological control measures (Germinara et al., 2008GERMINARA, G.S., CRISTOFARO, A. and ROTUNDO, G., 2008. Behavioral responses of adult Sitophilus granarius to individual cereals volatiles. Journal of Chemical Ecology, vol. 34, no. 4, pp. 523-529. http://dx.doi.org/10.1007/s10886-008-9454-y. PMid:18340486.
http://dx.doi.org/10.1007/s10886-008-945...
).

Synthetic insecticides are widely used against insect pests (Tapondjou et al., 2005TAPONDJOU, A.L., ADLER, C., FONTEM, D.A., BOUDA, H. and REICHMUTH, C., 2005. Bioactivities of cymol and essential oils of Cupressussem pervirens and Eucalyptus saligna against Sitophilus zeamais Motschulsky and Tribolium confusum du Val. Journal of Stored Products Research, vol. 41, no. 1, pp. 91-102. http://dx.doi.org/10.1016/j.jspr.2004.01.004.
http://dx.doi.org/10.1016/j.jspr.2004.01...
). These pesticides cause environmental pollution and develop resistant insect pests and high mammalian toxicity (Al-Moajel, 2000AL-MOAJEL, N.H., 2000. Turnip seed (Brassica napus) extracts as grain wheat protectants against the grainary weevil, Sitopltilus granarius L. Saudi Journal of Biological Sciences, vol. 7, no. 1, pp. 94-102.). Development of bio-insecticides has been an alternative strategy to use of synthetic pesticides (Hashim and Devi, 2003HASHIM, M.S. and DEVI, K.S., 2003. Insecticidal action of the polyphenolic rich fractions from the stem bark of Streblusasperon Dysdercuscingulalus. Fitoterapia, vol. 74, no. 7-8, pp. 670-676. http://dx.doi.org/10.1016/S0367-326X(03)00186-2. PMid:14630171.
http://dx.doi.org/10.1016/S0367-326X(03)...
; Meena et al., 2006MEENA, R., SUHAG, P. and PRATES, H.T., 2006. Evaluation of ethanolic extract of Baccharisgenistelloides against stored grain pests. Journal of Stored Products Research, vol. 34, no. 4, pp. 243-249.). In Asia a number of plant products have been traditionally used for protection of stored cereals (Isman, 2000ISMAN, M.B., 2000. Plant essential oils for pest and disease management. Crop Protection, vol. 19, no. 8-10, pp. 603-608. http://dx.doi.org/10.1016/S0261-2194(00)00079-X.
http://dx.doi.org/10.1016/S0261-2194(00)...
). Plants derivative pesticides are renewable, biodegradable and have low mammalian cytotoxicity (Isman, 2008ISMAN, M.B., 2008. Botanical insecticides: for richer, for poorer. Pest Management Science, vol. 64, no. 1, pp. 8-11. http://dx.doi.org/10.1002/ps.1470. PMid:18022796.
http://dx.doi.org/10.1002/ps.1470...
). Digestive enzymes convert complex biomolecules to simplest one (Erturk, 2006ERTURK, O., 2006. Antifeedant and toxicity effects of some plant extracts on thaumeto poaesolitaria Frey. (Lepidoptera: thaumetapoeidae). Turkish Journal of Biology, vol. 30, pp. 51-57.). Any disturbance in enzyme activity of insects is fatal for their survival (Shekari et al., 2008SHEKARI, M., SENDI, J.J., ETEBARI, K., ZIBAEE, A. and SHADPARVAR, A., 2008. Effects of Artemisia annua L. (Asteracea) on nutritional physiology and enzyme activities of elm leaf beetle, Xantho galerucaluteola Mull (Coleoptera: chrysomellidae). Pesticide Biochemistry and Physiology, vol. 91, no. 1, pp. 66-74. http://dx.doi.org/10.1016/j.pestbp.2008.01.003.
http://dx.doi.org/10.1016/j.pestbp.2008....
). Dehydrogenases are important tools for the investigation of insect metabolic activities during the course of development (Dickinson and Sullivan, 1975DICKINSON, W.J. and SULLIVAN, D.T., 1975. Gene enzyme system in Drosophila. Berlin: Springer.). Terra and Ferreira (2005)TERRA, W.R. and FERREIRA, C., 2005. Biochemistry of digestion. In: L.I. GILBERT, ed. Comprehensive molecular insect science. Amsterdam: Elsevier, pp. 171-224. http://dx.doi.org/10.1016/B0-44-451924-6/00053-3.
http://dx.doi.org/10.1016/B0-44-451924-6...
confirmed that Amylases are obligatory to digest carbohydrates in insects.

2. Material and Methods

2.1. Sampling area

The infested wheat grains with S. granarius were randomly collected from wheat stores of Mansehra and reared in the laboratory. Local wheat, Triticum aestivum was used for rearing of insect. The wheat used in the experiment was cleaned from insects by fumigation with Aluminum sulphate. Fresh, mature and unripen fruits of R. fruticosus were collected from Shatey, Mansehra. The rhizomes of V. jatamansi were collected from Kund Bangla, Mansehra, Pakistan (Figure 1).

Figure 1
(a) Plant of V. jatamansi; (b) dried rhizome of V. jatamansi; (c) Plant of R. fruticosus; (d) dried fruits of R. fruticosus.

2.2. Rearing of insects

Three hundred adult S. granarius were grown in 2-liter jar (14×13.6 cm) having 750 g purified wheat grains at a controlled temperature of 37 ± 2 °C and relative-humidity 60 ± 10% (Mehmood, 2007MEHMOOD, T., 2007. Toxicity and effect of crude plant extract, Solanum Surrattence on red flour beetle, Tribolium castanium. Kohat, Pakistan: Department of Zoology, Kohat University of Science and Technology. M. Sc Thesis in Zoology.). Each rearing jar was covered with muslin cloth for aeration.

2.3. Preparation of plant powders

Mature and unripened fruits of R. fruticosus and rhizome of V. jatamansi were collected, rinsed with distilled water and air dried in the laboratory at room temperature of 20 °C. Dried plant materials were grounded by electrical blender (Rehman et al., 2009REHMAN, J., JILLANI, G., KHAN, M., MASIH, R. and KANVIL, S., 2009. Repellent and oviposition detterent effects of indigenous plant extracts to peach fruit fly, Bactrocera zonata Saunders (Diptera: tephritidae). Pakistan Journal of Zoology, vol. 41, pp. 101-108.). The resulting powders were sieved, using 40 mesh screens and stored in cool and dry place to maintain efficacy.

2.4. Determination of malate dehydrogenase activity

The enzymatic activity of malate dehydrogenase (MDH) was observed in the cellular extract of S. granarius after treatment with R. fruticosus and V. jatamansi powders and compared with control. The experimental insects were crushed and homogenized in phosphate buffer (pH 7.0) solution using a mortar and pistol. Homogenates were centrifuged (Force 1624 microcentrifuge, Edison, NJ, USA) at 10000 rpm for 5 minutes. For the enzymatic measurement of malate dehydrogenase, supernatant was tested in spectrophotometer adjusted at 340 nm. The following solutions were added into the cuvette (1.4 mL Phosphate buffer (0.1M), 0.04 mL Cis-Oxaloacetic acid (0.006M) and 0.02 mL NADH (0.00375M). The reagents were mixed and incubated at 25 °C for five minutes. The cuvettes were placed in the experimental reference sites of spectrophotometer (Perkin Elmer lambd 25 UV/Visible, double-beam, Spectrophotometer, USA) for 2-3 minutes to achieve temperature equilibration, and pippeted 0.005 mL extract of insects into experimental cuvette, mixed it well and monitored the reaction for 2-3 minutes. The oxaloacetate and NADH is converted into L-Malate and NAD+ by the enzymatic action of Malate dehydrogenase:

MDH

Oxaloacetate + NADH → L-Malate + NAD+

The measurement of MDH activity was based on the rate of decline in the absorbance at wave length (λ) of 340 nm, subsequent to the oxidation of NADH. One enzyme unit is defined as the amount of enzyme which can catalyze the conversion of one µmole of oxaloacetate to malate per minute at 25 °C. The number of enzyme units per mL of cellular extract was calculated by using the Formula 1:

E n z y m e a c t i v i t y U / m L = A b s o r b a n c e c h a n g e × T o t a l v o l u m e m L × D F 6.22 × E n z y m e v o l u m e m L (1)

Whereas: DF = Dilution factor of enzyme; 6.22 = Extinction coefficient of NADH at 340 nm in milli moles (Worthington and Worthington, 2011WORTHINGTON, K. and WORTHINGTON, V., 2011 [viewed 15 Jan 2012]. Worthington enzyme manual [online]. Lakewood, NJ: Worthington Biochemical Corporation. Available from: http://www.worthington-biochem.com/pap/default.html
http://www.worthington-biochem.com/pap/d...
).

2.5. Determination of alpha amylase activity

Enzymes dilutions were prepared using Sodium Phosphate (Na3PO4) 0.02 M buffers at 6.9 pH for each strain separately in eppendorf tubes and kept in ice box. One gram of dinitosalicylic acid as color reagent was mixed in 20 mL of 2M sodium hydroxide (NaOH) and slowly added 30 g sodium potassium tartrate tetrahydrate and made final volume to 100 mL. One percent starch was dissolved in Sodium phosphate buffer (0.02M) having 0.006M sodium chloride (NaCl). 500 µL of 1% starch solution was mixed with 20 µL of cellular extract in triplicates. One ml of the salicylic acid solution was added to each reaction mixture and boiled for five minutes. The reacted samples were cooled to room temperature and added 10 µL of distilled to each tube (making 6.66 time dilution). The absorbance of diluted reaction mixture was measured at 540 nm and compared with standard curve of maltose for the determination of µ-moles of maltose liberated in the reaction. A unit of amylase is defined as the amount of enzyme which can liberate one µ-moles of maltose from starch in one minute (Worthington and Worthington, 2011WORTHINGTON, K. and WORTHINGTON, V., 2011 [viewed 15 Jan 2012]. Worthington enzyme manual [online]. Lakewood, NJ: Worthington Biochemical Corporation. Available from: http://www.worthington-biochem.com/pap/default.html
http://www.worthington-biochem.com/pap/d...
). The activity of enzyme was calculated as follows (Formula 2):

E n z y m e a c t i v i t y U / m L = µ m o l e s o f m a l t o s e l i b e r a t e d p e r m i n u t e V o l u m e o f e n z y m e a d d e d m L (2)

3. Results

The reduction in malate dehydrogenase activity for R. fruticosus and V.jatamansi against S. granarius revealed a decrease in the levels of enzyme by 5.60% and 14.92% respectively, compared with that of control (Table 1).

Table 1
Reduction in malate dehydrogenase activity for R. fruticosus and V. jatamansi against S. granarius.

The activity level of amylase in the extract of R. fruticosus and V. jatamansi treated insects showed 6.82% decrease and 63.63% increase respectively. The results represented a significant decrease in the α-amylase activity in V. jatamansi treated insects while a modified activity was observed in R. fruticosus treated S. granarius (Table 2).

Table 2
Alteration in alpha amylase activity for R. fruticosus and V. jatamansi against S.granarius.

4. Discussion

This study was carried out from May-September, 2011 to assess the efficacy of two plant powders R. fruticosus and V.jatamansi against S. granarius and changes in the enzyme activities. Both the plant powders were collected from different localities of Mansehra Pakistan and were used as treatment against the granary weevil.

In the present study the malate dehydrogenase enzyme activity in R. fruticosus and V. jatamansi treated S. granarius was reduced by 5.60% and 14.92% respectively, compared with that of control. In the previous studies of Hamadah et al. (2010)HAMADAH, K.S., BASIOUNY, A.L. and GHONEIM, K.S., 2010. Alterations in the lactate dehydrogenase activity of the desert locust S. gregaria by the wild plant Fagonia bruguieri (Zygophyllaceae). Academic. The Journal of Biological Sciences, vol. 3, no. 2, pp. 1-9. the alterations in the dehydrogenase activity of the desert locust Schistocerca gregaria was observed, the wild plant Fagonia bruguieri changed the enzyme activity +0.5% in the early-aged nymphs at the lower concentration level of petroleum ether extract along the nymphal instar but the strongest enhancing effect was exhibited in the mid-aged nymphs.

In the present study the α-amylase enzyme activity in R. fruticosus and V. jatamansi treated S. granarius 6.82% decrease and 63.63% increase respectively. Earlier Nehad et al. (2008)NEHAD, M.E., HUSSAIN, F.D. and YASSER, A.E., 2008. Toxicological evaluation and biochemical impacts for radient as a new generation of spinosyn on spodopteralittoralis (Boisd.) larvae. Egyyptin Academy Journal of Biological Sciences, vol. 2, pp. 85-97. reported that activity of amylase was decreased after 24h of plant extract treatment. Mehrabadi et al. (2011)MEHRABADI, M., BANDANI, A.R., SAADATI, F. and MAHMUDVAND, M., 2011. α amylase activity of stored products insects and its inhibition by medicinal plant extracts. Journal of Agricultural Science and Technology, vol. 13, pp. 1173-1182. reported Inhibitory effect of plants extracts of A. Siberia, P. harmala, and T. vulgaris against C. maculatus showed the reduced amylase activity 19.22%, 4.58%, and 7.22% respectively. Ahmad et al. (2019)AHMAD, F., IQBAL, N., ZAKA, S.M., QURESHI, M.K., SAEED, Q., KHAN, K.A., GHRAMH, H.A., ANSARI, M.J., JALEEL, W., AASIM, M. and AWAR, M.B., 2019. Comparative insecticidal activity of different plant materials from six common plant species against Tribolium castaneum (Herbst) (Coleoptera:Tenebrionidae). Saudi Journal of Biological Sciences, vol. 26, no. 7, pp. 1804-1808. http://dx.doi.org/10.1016/j.sjbs.2018.02.018. PMid:31762662.
http://dx.doi.org/10.1016/j.sjbs.2018.02...
used different plant powders against T. castaneum infesting stored grains. Allium sativum and Zingeber officinale were more effective resulting into 15 time’s higher adult mortality. The Azadirachta indica seed powder against the beetle showed better control at lowest (1% w/w) and the highest doses (5% w/w).

Acknowledgements

Dr. Muhammad Shahid Nadeem is appreciated to accomplish my enzyme assay on the bio-pesticides, treated insects.

  • (With 1 figure)

References

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  • NEHAD, M.E., HUSSAIN, F.D. and YASSER, A.E., 2008. Toxicological evaluation and biochemical impacts for radient as a new generation of spinosyn on spodopteralittoralis (Boisd.) larvae. Egyyptin Academy Journal of Biological Sciences, vol. 2, pp. 85-97.
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    » http://dx.doi.org/10.1016/j.pestbp.2008.01.003
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    » http://dx.doi.org/10.1016/j.jcs.2007.06.006
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    » http://dx.doi.org/10.1016/B0-44-451924-6/00053-3
  • UDO, I.O., 2011. Potentials of Zanthoxylum xanthoxyloides (LAM.) for the control of stored product insect pests. Journal of Stored Products and Postharvest Research, vol. 2, no. 3, pp. 40-44.
  • WORTHINGTON, K. and WORTHINGTON, V., 2011 [viewed 15 Jan 2012]. Worthington enzyme manual [online]. Lakewood, NJ: Worthington Biochemical Corporation. Available from: http://www.worthington-biochem.com/pap/default.html
    » http://www.worthington-biochem.com/pap/default.html

Publication Dates

  • Publication in this collection
    01 June 2020
  • Date of issue
    Mar-May 2021

History

  • Received
    16 Aug 2019
  • Accepted
    27 Nov 2019
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