Sains Malaysiana 53(10)(2024): 3341-3354

http://doi.org/10.17576/jsm-2024-5310-09

 

Comprehensive Insights into Sitobion avenaePreferences and Performance on Pakistan’s Wheat Cultivars Leading to Identification of Potential RNAi Targets

(Wawasan Komprehensif tentang Keutamaan dan Prestasi Sitobion avenae pada Kultivar Gandum Pakistan yang Membawa kepada Pengenalpastian Sasaran Berpotensi RNAi)

 

RUHMA MUKHTAR, EIJAB AFZAL, RABIA NOREEN, NADIA ZEESHAN & AMBER AFROZ*

 

Department of Biochemistry and Biotechnology, University of Gujrat, Hafiz Hayat Campus, Gujrat Pakistan

 

Diserahkan: 14 Januari 2024/Diterima: 26 Ogos 2024

 

Abstract

Sitobion avenae, a notable hemipteran pest, poses a significant economic threat to Triticum aestivum due to its short generation times and high reproductive rates. Challenges like the development of insecticide resistance, the limited impact of insecticidal genes, and associated risks led to seeking a more precise approach like RNA interference. This study evaluated S. avenae response on seven different local cultivars (Anaj-2021, Subhani-2022, Fakhar-e-Bhakkar-2021, Akbar-2019, Mexi-Pak-2022, Barani-2022, & Dilkash-2022) through aphid preference test, aphid choice assay, and aphid performance test. Further, differential proteomics of S. avenae (pre- and post-feeding on susceptible and resistant wheat cultivars) was performed using Sodium Dodecyl Sulphate-Polyacrylamide Gel Electrophoresis. Among the local wheat cultivars, Anaj-2021 was regarded as the most susceptible cultivar while Barani-2022 was declared the most resistant. The differential proteome analysis of Anaj-2021 (S), and Barani-2022 (R) show 11 upregulated proteins including Glutathione S- transferase, Cathepsin, Carbonic anhydrases, Ecdysone induced protein, Odorant binding protein 3, Heat shock protein, Salivary effector protein, SID1-like protein, Sodium channel protein, chemosensory protein, and trypsin were upregulated in S. avenaeon wheat feeding as compared to non-feeding. Trypsin, cathepsin-B and carbonic anhydrases are connected to detoxification and digestion. While odorant binding proteins, salivary effector proteins, sodium channel proteins and ecdysone- induced proteins facilitate feeding process in S. avenae. The enhanced expression of proteins having detoxification, digestion or defense activity implicates their essential role in the survival of S. avenae. Therefore, these proteins have the potential to serve as RNA interference targets, against which double-stranded RNA could be designed and expressed in wheat cultivars to make them resistant to local S. avenae infestation and avert yield loss.

 

Keywords: Phylogenetic analysis; proteome; RNA interference; SDS-PAGE

 

Abstrak

Sitobion avenae, perosak hemiptera yang terkenal menimbulkan ancaman ekonomi yang ketara kepada Triticum aestivum kerana masa generasinya yang singkat dan kadar pembiakan yang tinggi. Cabaran seperti pembangunan rintangan racun serangga, kesan terhad gen insektisida dan risiko yang berkaitan membawa kepada mencari pendekatan yang lebih tepat seperti gangguan RNA. Kajian ini menilai tindak balas S. avenae pada tujuh kultivar tempatan yang berbeza (Anaj-2021, Subhani-2022, Fakhar-e-Bhakkar-2021, Akbar-2019, Mexi-Pak-2022, Barani-2022 & Dilkash-2022) melalui aphid ujian keutamaan, ujian pilihan aphid dan ujian prestasi aphid. Selanjutnya, proteomik pembezaan S. avenae (sebelum dan selepas makan pada kultivar gandum yang mudah terdedah dan tahan) dilakukan menggunakan Sodium Dodecyl Sulphate-Polyacrylamide Gel Electrophoresis. Antara kultivar gandum tempatan, Anaj-2021 dianggap sebagai kultivar yang paling mudah terdedah manakala Barani-2022 diisytiharkan paling tahan. Analisis proteom pembezaan Anaj-2021 (S) dan Barani-2022 (R) menunjukkan 11 protein terkawal termasuk Glutathione S- transferase, Cathepsin, Carbonic anhydrases, Ecdysone induced protein, Odorant binding protein 3, Heat shock protein, Salivary effector protein, protein seperti SID1, protein saluran Sodium, protein kemoderia dan tripsin telah dikawal selia dalam S. avenae pada pemberian makan gandum berbanding dengan tidak diberi makan. Trypsin, cathepsin-B dan anhidrase karbonik disambungkan kepada detoksifikasi dan pencernaan. Manakala protein pengikat bau, protein efektor air liur, protein saluran natrium dan protein yang disebabkan oleh ecdysone memudahkan proses penyusuan di S. avenae. Pengekspresan protein yang dipertingkatkan mempunyai aktiviti detoksifikasi, pencernaan atau pertahanan membabitkan peranan pentingnya dalam kemandirian S. avenae. Oleh itu, protein ini berpotensi untuk berfungsi sebagai sasaran gangguan RNA yang terhadapnya RNA untai dua boleh direka bentuk dan diekspresikan dalam kultivar gandum untuk menjadikannya tahan terhadap serangan S. avenae tempatan dan mengelakkan kehilangan hasil.

 

Kata kunci: Analisis filogenetik; gangguan RNA; proteome; SDS-PAGE

 

RUJUKAN

Afroz, A., Ali, G.M., Mir, A. & Komatsu, S. 2011. Application of proteomics to investigate stress-induced proteins for improvement in crop protection. Plant Cell Reports 30: 745-763.

Afzal, F., Chaudhari, S.K., Gul, A., Farooq, A., Ali, H., Nisar, S., Sarfraz, B., Shehzadi, K.J. &  Mujeeb-Kazi, A. 2015. Bread wheat (Triticum aestivum L.) under biotic and abiotic stresses: An overview. In Crop Production and Global Environmental Issues, edited by Hakeem, K. Springer, Cham. pp. 293-317.

Akhremko, A., Vasilevskaya, E. & Fedulova, L. 2020. Adaptation of two-dimensional electrophoresis for muscle tissue analysis. Slovak Journal of Food Sciences 14: 595-601.

Akhtar, N., Hashmat, R.T., Jilani, G., Chughtai, S., Irshad, M. & Yasmin, S. 2007. Resistance of different wheat lines to Rhopalosiphum padi (L.)(Aphididae: Homoptera) in Pakistan. Pakistan Journal of Zoology 39(3): 191-194.

Awmack, C.S. & Leather, S.R. 2002. Host plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47: 817-844.

Bansal, R. & Michel, A.P. 2013. Core RNAi machinery and Sid1, a component for systemic RNAi, in the hemipteran insect, Aphis glycines. International Journal of Molecular Sciences 14(2): 3786-3801.

Buhler, A. & Schweiger, R. 2023. Previous infestation by conspecifics leads to a transient increase of the performance of Sitobion avenae aphids on wheat leaves. Ecological Entomology 49: 476-488. doi: 10.1111/een.13316

Cai, Q., Zhang, Q. & Cheo, M. 2004. Contribution of indole alkaloids to Sitobion avenae (F.) resistance in wheat. Journal of Applied Entomology 128(8): 517-521.

Cao, H-H., Pan, M-Z., Liu, H-R., Wang, S-H. & Liu, T-X. 2015. Antibiosis and tolerance but not antixenosis to the grain aphid, Sitobion avenae (Hemiptera: Aphididae), are essential mechanisms of resistance in a wheat cultivar. Bulletin of Entomological Research 105(4): 448-455.

Cao, H-H., Zhang, M., Zhao, H., Zhang, Y., Wang, X-X., Guo, S-S., Zhang, Z-F. & Liu, T-X. 2014. Deciphering the mechanism of β-aminobutyric acid-induced resistance in wheat to the grain aphid, Sitobion avenae. PLoS ONE 9(3): e91768.

Castro, A.M., Vasicek, A., Manifiesto, M., Giménez, D., Tacaliti, M.S., Dobrovolskaya, O., Röder, M.S., Snape, J.W. & Börner, A. 2005. Mapping antixenosis genes on chromosome 6A of wheat to greenbug and to a new biotype of Russian wheat aphid. Plant Breeding 124(3): 229-233.

De Mandal, S., Chhakchhuak, L., Gurusubramanian, G. & Kumar, N.S. 2014. Mitochondrial markers for identification and phylogenetic studies in insects - A review. DNA Barcodes 2(1): 1-9.

Dembilio, Ó., Jacas, J.A. & Llácer, E. 2009. Are the palms Washingtonia filifera and Chamaerops humilis suitable hosts for the red palm weevil, Rhynchophorus ferrugineus (Col. Curculionidae)? Journal of Applied Entomology 133(7): 565-567.

Deng, F. & Zhao, Z. 2014. Influence of catalase gene silencing on the survivability of Sitobion avenae. Archives of Insect Biochemistry and Physiology 86(1): 46-57.

Douglas, A. 2006. Phloem-sap feeding by animals: Problems and solutions. Journal of Experimental Botany 57(4): 747-754.

Feng, H., Chen, W., Hussain, S., Shakir, S., Tzin, V., Adegbayi, F., Ugine, T., Fei, Z. & Jander, G. 2023. Horizontally transferred genes as RNA interference targets for aphid and whitefly control. Plant Biotechnology Journal 21(4): 754-768.

Foster, S.P., Paul, V.L., Slater, R., Warren, A., Denholm, I., Field, L.M. & Williamson, M.S. 2014. A mutation (L1014F) in the voltage‐gated sodium channel of the grain aphid, Sitobion avenae, is associated with resistance to pyrethroid insecticides. Pest Management Science 70(8): 1249-1253.

Gebretsadik, K.G., Zhang, Y. & Chen, J. 2022. Screening and evaluation for antixenosis resistance in wheat accessions and varieties to grain aphid, Sitobion miscanthi (Takahashi)(Hemiptera: Aphididae). Plants 11(8): 1094.

Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Faucher, M. & Bonnemain, J-L. 2010. Compatible plant-aphid interactions: How aphids manipulate plant responses. Comptes Rendus Biologies 333(6-7): 516-523.

Guo, H., Zhang, Y., Li, B., Li, C., Shi, Q., Zhu-Salzman, K., Ge, F. & Sun, Y. 2023. Salivary carbonic anhydrase II in winged aphid morph facilitates plant infection by viruses. Proceedings of the National Academy of Sciences 120(14): e2222040120.

Guo, M., Ye, J., Gao, D., Xu, N. & Yang, J. 2019. Agrobacterium-mediated horizontal gene transfer: Mechanism, biotechnological application, potential risk and forestalling strategy. Biotechnology Advances 37(1): 259-270.

He, F. 2011. Bradford protein assay. Bio-protocol 1(6): e45.

Hesler, L. & Tharp, C. 2005. Antibiosis and antixenosis to Rhopalosiphum padi among triticale accessions. Euphytica 143: 153-160.

Horiike, T. 2016. An introduction to molecular phylogenetic analysis. Reviews in Agricultural Science 4: 36-45.

Hu, X-S., Liu, Y-J., Wang, Y-H., Wang, Z., Yu, X-L., Wang, B., Zhang, G-S., Zhao, H-Y. & Liu, T.X. 2016. Resistance of wheat accessions to the English grain aphid Sitobion avenae. PLoS ONE 11(6): e0156158.

Hussain, D., Asrar, M., Khalid, B., Hafeez, F., Saleem, M., Akhter, M., Ahmed, M., Ali, I. & Hanif, K. 2022. Insect pests of economic importance attacking wheat crop (Triticum aestivum L.) in Punjab, Pakistan. International Journal of Tropical Insect Science 42: 9-20.

Huvenne, H. & Smagghe, G. 2010. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: A review. Journal of Insect Physiology 56(3): 227-235.

Jacquin-Joly, E., Vogt, R.G., François, M-C. & Nagnan-Le Meillour, P. 2001. Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chemical Senses 26(7): 833-844.

Kranti, W., Nivedita, G. & Shindikar, M. 2021. Understanding the plant aphid interaction: A review. European Journal of Biology and Biotechnology 2(6): 1-6.

Kurreck, J. 2009. RNA interference: From basic research to therapeutic applications. Angewandte Chemie International Edition 48(8): 1378-1398.

Leimu, R. & Koricheva, J. 2006. A meta-analysis of genetic correlations between plant resistances to multiple enemies. The American Naturalist 168(1): E15-E37.

Liu, Y-L., Guo, H., Huang, L-Q., Pelosi, P. & Wang, C-Z. 2014. Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. Journal of Experimental Biology 217(10): 1821-1826.

Mahmood, I., Afroz, A., Malik, M.F., Zeeshan, N., Khan, M.R., Rashid, U., Khan, M.A., Ashraf, N.M. & Alam, S. 2022. RNA interference‑mediated knockdown of odorant‑binding protein 2 and MP58 gene causes mortality in Myzus persicae. International Journal of Tropical Insect Sciences 42: 315-326. doi.10.1007/s42690-021-00546-z

Nam, K.J., Powell, G. & Hardie, J. 2013. Does phloem-based resistance to aphid feeding affect host-plant acceptance for reproduction? Parturition of the pea aphid, Acyrthosiphon pisum, on two near-isogenic lines of Medicago truncatula. Bulletin of Entomological Research 103(6): 683-689.

Platková, H., Skuhrovec, J. & Saska, P. 2020. Antibiosis to Metopolophium dirhodum (Homoptera: Aphididae) in spring wheat and emmer cultivars. Journal of Economic Entomology 113(6): 2979-2985.

Porcar, M., Grenier, A-M., Federici, B. & Rahbé, Y. 2009. Effects of Bacillus thuringiensis δ-endotoxins on the pea aphid (Acyrthosiphon pisum). Applied and Environmental Microbiology 75(14): 4897-4900.

Powell, G., Tosh, C.R. & Hardie, J. 2006. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 51: 309-330.

Pyati, P., Bandani, A.R., Fitches, E. & Gatehouse, J.A. 2011. Protein digestion in cereal aphids (Sitobion avenae) as a target for plant defence by endogenous proteinase inhibitors. Journal of Insect Physiology 57(7): 881-891.

Roy, S.S., Dasgupta, R. & Bagchi, A. 2014. A review on phylogenetic analysis: A journey through modern era. Computational Molecular Bioscience 4: 39-45.

Shafqat, J. & Afroz, A. 2024a. RNA interference of Sitobion avenae voltage-gated sodium channels for improved grain aphid resistance. International Journal of Tropical Insect Science 44: 1679-1689. doi.10.1007/s42690-024-01261-1

Shafqat, J. & Afroz, A. 2024b. Differential protein expression analysis of wheat cultivars and grain aphids post-feeding. Journal of Tianjin University Science and Technology 57(1): 143-164. doi.10.5281/zenodo.10612560

Smith, C.M. & Chuang, W.P. 2014. Plant resistance to aphid feeding: Behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Management Science 70(4): 528-540.

Sreelatha, E., Sharma, H. & Gowda, C. 2018. Tolerance as mechanism of resistance to Helicoverpa armigera (Hub.) in Chickpea (Cicer arietinum Linn.). Trends in Biosciences 11(2): 144-148.

Tabari, M., Fathi, S., Nouri-Ganbalani, G., Moumeni, A. & Razmjou, J. 2017. Antixenosis and antibiosis resistance in rice cultivars against Chilo suppressalis (Walker)(Lepidoptera: Crambidae). Neotropical Entomology 46: 452-460.

Vellichirammal, N.N., Gupta, P., Hall, T.A. & Brisson, J.A. 2017. Ecdysone signaling underlies the pea aphid transgenerational wing polyphenism. Proceedings of the National Academy of Sciences 114(6): 1419-1423.

Wains, M.S., Javaid, M.M., Afzal, M.B.S., Ali, H.A., Sarfraz, M., Banazeer, A., Hussain, F. & Aslam, M.N. 2023. Surveillance and evaluation of climatic factors on varietal screening against aphid population in wheat. Pakistan Journal of Biotechnology 20(02): 371-375.

Webster, B. 2012. The role of olfaction in aphid host location. Physiological Entomology 37(1): 10-18.

Wyatt, I. & White, P. 1977. Simple estimation of intrinsic increase rates for aphids and tetranychid mites. Journal of Applied Ecology 14(3): 757-766.

Xu, W. & Han, Z. 2008. Cloning and phylogenetic analysis of sid-1-like genes from aphids. Journal of Insect Science 8: 1-6.

Xue, W., Fan, J., Zhang, Y., Xu, Q., Han, Z., Sun, J. & Chen, J. 2016. Identification and expression analysis of candidate odorant-binding protein and chemosensory protein genes by antennal transcriptome of Sitobion avenae. PLoS ONE 11(8): e0161839.

Yu, X., Wang, G., Huang, S., Ma, Y. & Xia, L. 2014. Engineering plants for aphid resistance: Current status and future perspectives. Theoretical and Applied Genetics 127: 2065-2083.

Yu, X.D., Liu, Z.C., Huang, S.L., Chen, Z.Q., Sun, Y.W., Duan, P.F., Ma, Y.Z. & Xia, L.Q. 2016. RNAi‐mediated plant protection against aphids. Pest Management Science 72(6): 1090-1098.

Zeb, Q., Naeem, M., Khan, S.A. & Ahmad, S. 2016. Effect of insecticides on the population of aphids, natural enemies and yield components of wheat. Pakistan Journal of Zoology 48(6): 1839-1848.

Zhang, N., Liu, D., Zhai, Y., Li, X. & Simon, J.C. 2022. Functional divergence of three glutathione transferases in two biotypes of the English grain aphid, Sitobion avenae. Entomologia Experimentalis et Applicata 170(1): 79-87.

Zhang, Y., Fan, J., Francis, F. & Chen, J. 2018. Molecular characterization and gene silencing of Laccase 1 in the grain aphid, Sitobion avenae. Arch. Insect Biochem. Physiol. 97(4): e21446. https://doi.org/10.1002/arch.21446

Zhang, M., Zhou, Y., Wang, H., Jones, H.D., Gao, Q., Wang, D., Ma, Y. & Xia, L. 2013. Identifying potential RNAi targets in grain aphid (Sitobion avenae F.) based on transcriptome profiling of its alimentary canal after feeding on wheat plants. BMC Genomics 14: 560.

 

*Pengarang untuk surat-menyurat; email: dramber.afroz@uog.edu.pk

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

sebelumnya