Insecticidal proteins and their potential use for Colorado potato beetle (Leptinotarsa decemlineata [Say, 1824]) control

Authors

  • Primož ŽIGON Agricultural institute of Slovenia, Slovenia
  • Jaka RAZINGER Agricultural institute of Slovenia, Slovenia
  • Stanislav TRDAN University of Ljubljana, Slovenia

DOI:

https://doi.org/10.14720/aas.2021.117.3.2221

Keywords:

entomotoxic proteins, bioinsecticide, plant toxins, potato, insecticide resistance

Abstract

Plants respond to pest attack, among other mechanisms, by producing specific proteins with insecticidal properties. Proteins with toxic effects on insects have also been discovered in many other organisms, especially fungi and bacteria. Due to their biological function, insecticidal proteins represent an important potential in the development of more environmentally friendly plant protection methods. Increasing knowledge about the mode of action of insecticidal proteins and the identification of genes encoding their synthesis enable the breeding of transgenic plants resistant to insect pests and the development of new bioinsecticidal agents. The Colorado potato beetle (Leptinotarsa decemlineata) is one of the most important pests of potato, so the study of such control methods is crucial for the development of sustainable integrated pest management strategies of potato. This review highlights the properties of some groups of insecticidal proteins and their modes of action, and summarizes examples of studies of their use for the control of Colorado potato beetle.

Author Biographies

  • Primož ŽIGON, Agricultural institute of Slovenia, Slovenia
    Plant protection department, research assistant
  • Jaka RAZINGER, Agricultural institute of Slovenia, Slovenia
    Plant protection department, researcher
  • Stanislav TRDAN, University of Ljubljana, Slovenia
    Department of Agronomy, University professor

     

     

References

Álvarez-Alfageme, F., Martínez, M., Pascual-Ruiz, S., Castañera, P., Diaz, I., Ortego, F. (2007). Effects of potato plants expressing a barley cystatin on the predatory bug Podisus maculiventris via herbivorous prey feeding on the plant. Transgenic Research, 16(1), 1–13. https://doi.org/10.1007/s11248-006-9022-6

Alyokhin, A., Baker, M., Mota-Sanchez, D., Dively, G., Grafius, E. (2008). Colorado potato beetle resistance to insecticides. American Journal of Potato Research, 85(6), 395–413. https://doi.org/10.1007/s12230-008-9052-0

Ashouri, S., Farshbaf Pourabad, R. (2021). Regulation of gene expression encoding the digestive α-amylase in the larvae of Colorado potato beetle, Leptinotarsa decemlineata (Say) in response to plant protein extracts. Gene, 766, 145159. https://doi.org/10.1016/j.gene.2020.145159

Ashouri, S., Farshbaf Pourabad, R., Kocadağ Kocazorbaz, E., Zihnioglu, F. (2017). Influence of red kidney bean seed proteins on development, digestive α-amylase activity and gut protein pattern of Leptinotarsa decemlineata (Say). Journal of the Entomological Research Society, 19(3), 69–83.

Balaško, M. K., Mikac, K. M., Bažok, R., Lemic, D. (2020). Modern techniques in colorado potato beetle (Leptinotarsa decemlineata Say) control and resistance management: History review and future perspectives. Insects, 11(9), 1–17. https://doi.org/10.3390/insects11090581

Berne, S., Lah, L., Sepčić, K. (2009). Aegerolysins: Structure, function, and putative biological role. Protein Science, 18(4), 694–706. https://doi.org/10.1002/pro.85

Berry, C., Crickmore, N. (2017). Structural classification of insecticidal proteins – Towards an in silico characterisation of novel toxins. Journal of Invertebrate Pathology, 142, 16–22. https://doi.org/10.1016/j.jip.2016.07.015

Blackburn, M. B., Domek, J. M., Gelman, D. B., Hu, J. S. (2005). The broadly insecticidal Photorhabdus luminescens toxin complex a (Tca): Activity against the Colorado potato beetle, Leptinotarsa decemlineata, and sweet potato whitefly, Bemisia tabaci. Journal of Insect Science, 5. https://doi.org/10.1093/jis/5.1.32

Bohinc, T., Vučajnk, F., Trdan, S. (2019). The efficacy of environmentally acceptable products for the control of major potato pests and diseases. Zemdirbyste-Agriculture, 106(2), 135–142. https://doi.org/10.13080/z-a.2019.106.018

Bravo, A., Gill, S. S., Soberón, M. (2007). Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon : official journal of the International Society on Toxinology, 49(4), 423—435. https://doi.org/10.1016/j.toxicon.2006.11.022

Bravo, A., Likitvivatanavong, S., Gill, S. S., Soberón, M. (2011). Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochemistry and Molecular Biology, 41(7), 423–431. https://doi.org/10.1016/j.ibmb.2011.02.006

Brunelle, F., Cloutier, C., Michaud, D. (2004). Colorado potato beetles compensate for tomato cathepsin D inhibitor expressed in transgenic potato. Archives of Insect Biochemistry and Physiology, 55(3), 103–113. https://doi.org/10.1002/arch.10135

Butala, M., Novak, M., Kraševec, N., Skočaj, M., Veranič, P., Maček, P., Sepčić, K. (2017). Aegerolysins: Lipid-binding proteins with versatile functions. Seminars in Cell and Developmental Biology, 72, 142–151). https://doi.org/10.1016/j.semcdb.2017.05.002

Carlini, C. R., Grossi-De-Sá, M. F. (2002). Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon, 40(11), 1515–1539. https://doi.org/10.1016/S0041-0101(02)00240-4

Chakroun, M., Banyuls, N., Bel, Y., Escriche, B., Ferré, J. (2016). Bacterial Vegetative Insecticidal Proteins (Vip) from Entomopathogenic Bacteria. Microbiology and Molecular Biology Reviews, 80(2), 329 LP – 350. https://doi.org/10.1128/MMBR.00060-15

Chen, M. S., Johnson, B., Wen, L., Muthukrishnan, S., Kramer, K. J., Morgan, T. D., Reeck, G. R. (1992). Rice cystatin: Bacterial expression, purification, cysteine proteinase inhibitory activity, and insect growth suppressing activity of a truncated form of the protein. Protein Expression and Purification, 3(1), 41–49. https://doi.org/10.1016/1046-5928(92)90054-Z

Cingel, A., Savić, J., Lazarević, J., Ćosić, T., Raspor, M., Smigocki, A., Ninković, S. (2016). Extraordinary adaptive plasticity of colorado potato beetle: “Ten-striped Spearman” in the era of biotechnologicalwarfare. International Journal of Molecular Sciences, 17(9). MDPI AG. https://doi.org/10.3390/ijms17091538

Cingel, A., Savić, J., Lazarević, J., Ćosić, T., Raspor, M., Smigocki, A., Ninković, S. (2017). Co-expression of the proteinase inhibitors oryzacystatin I and oryzacystatin II in transgenic potato alters Colorado potato beetle larval development. Insect Science, 24(5), 768–780. https://doi.org/https://doi.org/10.1111/1744-7917.12364

Cloutier, C., Jean, C., Fournier, M., Yelle, S., Michaud, D. (2000). Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Archives of Insect Biochemistry and Physiology, 44(2), 69–81. https://doi.org/10.1002/1520-6327(200006)44:2<69::AID-ARCH2>3.0.CO;2-6

Cooper, S. G., Douches, D. S., Grafius, E. J. (2009). Combining engineered resistance, avidin, and natural resistance derived from & lt; I & gt; Solanum chacoense & lt;/I & gt; bitter to control Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 102(3), 1270–1280. https://doi.org/10.1603/029.102.0354

Crickmore, N., Zeigler, D. R., Feitelson, J., Schnepf, E., Van Rie, J., Lereclus, D., Baum, J., Dean, D. H. (1998). Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiology and Molecular Biology Reviews, 62(3), 807–813. https://doi.org/10.1128/mmbr.62.3.807-813.1998

Dang, L., Van Damme, E. J. M. (2015). Toxic proteins in plants. Phytochemistry, 117(1), 51–64). https://doi.org/10.1016/j.phytochem.2015.05.020

Domínguez-Arrizabalaga, M., Villanueva, M., Escriche, B., Ancín-Azpilicueta, C., Caballero, P. (2020). Insecticidal activity of Bacillus thuringiensis proteins againstcoleopteran Pests. Toxins, 12(7), 430. https://doi.org/10.3390/toxins12070430

Donovan, W. P., Engleman, J. T., Donovan, J. C., Baum, J. A., Bunkers, G. J., Chi, D. J., Clinton, W. P., English, L., Heck, G. R., Ilagan, O. M., Krasomil-Osterfeld, K. C., Pitkin, J. W., Roberts, J. K., Walters, M. R. (2006). Discovery and characterization of Sip1A: A novel secreted protein from Bacillus thuringiensis with activity against coleopteran larvae. Applied Microbiology and Biotechnology, 72(4), 713–719. https://doi.org/10.1007/s00253-006-0332-7

Erjavec, J., Kos, J., Ravnikar, M., Dreo, T., Sabotič, J. (2012). Proteins of higher fungi - from forest to application. Trends in Biotechnology, 30(5), 259–273. https://doi.org/10.1016/j.tibtech.2012.01.004

Franco, O. L., Rigden, D. J., Melo, F. R., Grossi-de-Sá, M. F. (2002). Plant α-amylase inhibitors and their interaction with insect α-amylases. European Journal of Biochemistry, 269(2), 397–412. https://doi.org/https://doi.org/10.1046/j.0014-2956.2001.02656.x

Fürstenberg-Hägg, J., Zagrobelny, M., Bak, S. (2013). Plant defense against insect herbivores. International Journal of Molecular Sciences, 14(5), 10242–10297. https://doi.org/10.3390/ijms140510242

Gatehouse, A. M. R., Dewey, F. M., Dove, J., Fenton, K. A., Pusztai, A. (1984). Effect of seed lectins from Phaseolus vulgaris on the development of larvae of Callosobruchus maculatus; mechanism of toxicity. Journal of the Science of Food and Agriculture, 35(4), 373–380. https://doi.org/https://doi.org/10.1002/jsfa.2740350402

Grafius, E. J., Douches, D. S. (2008). The present and future role of insect-resistant genetically modified potato cultivars in IPM. V Integration of Insect-Resistant Genetically Modified Crops within IPM Programs (str. 195–221). Springer Netherlands. https://doi.org/10.1007/978-1-4020-8373-0_7

Green, T. R., Ryan, C. A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science, 175(4023), 776–777. https://doi.org/10.1126/science.175.4023.776

Gruden, K., Kuipers, A. G. J., Gunčar, G., Slapar, N., Štrukelj, B., Jongsma, M. A. (2004). Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases. Insect Biochemistry and Molecular Biology, 34(4), 365–375. https://doi.org/10.1016/j.ibmb.2004.01.003

Gruden, K., Štrukelj, B., Popovič, T., Lenarčič, B., Bevec, T., Brzin, J., Kregar, I., Herzog-Velikonja, J., Stiekema, W. J., Bosch, D., Jongsma, M. A. (1998). The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type-1 domain inhibitors. Insect Biochemistry and Molecular Biology, 28(8), 549–560. https://doi.org/10.1016/S0965-1748(98)00051-4

Jallouli, W., Driss, F., Fillaudeau, L., Rouis, S. (2020). Review on biopesticide production by Bacillus thuringiensis subsp. kurstaki since 1990: Focus on bioprocess parameters. V Process Biochemistry (Let. 98, str. 224–232). Elsevier Ltd. https://doi.org/10.1016/j.procbio.2020.07.023

Kalha, C. S., Singh, P. P., Kang, S. S., Hunjan, M. S., Gupta, V., Sharma, R. (2014). Entomopathogenic viruses and bacteria for insect-pest control. V Integrated Pest Management: Current Concepts and Ecological Perspective (str. 225–244). Elsevier Inc. https://doi.org/10.1016/B978-0-12-398529-3.00013-0

Kamionskaya, A. M., Kuznetsov, B. B., Ismailov, V. Y., Nadikta, V. D., Skryabin, K. G. (2012). Genetically transforming Russian potato cultivars for resistance to Colorado beetle. Clon Transgen, 1, 101. https://doi.org/10.4172/2168-9849.1000101

Lalitha, S., Shade, R. E., Murdock, L. L., Bressan, R. A., Hasegawa, P. M., Nielsen, S. S. (2005). Effectiveness of recombinant soybean cysteine proteinase inhibitors against selected crop pests. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology, 140(2), 227–235. https://doi.org/10.1016/j.cca.2005.02.007

Laznik, Ž., Tóth, T., Lakatos, T., Vidrih, M., Trdan, S. (2010). Control of the Colorado potato beetle (Leptinotarsa decemlineata [Say]) on potato under field conditions: a comparison of the efficacy of foliar application of two strains of Steinernema feltiae (Filipjev) and spraying with thiametoxam. Journal of Plant Diseases and Protection, 117(3), 129–135. https://doi.org/10.1007/BF03356348

Lecardonnel, A., Chauvin, L., Jouanin, L., Beaujean, A., Prévost, G., Sangwan-Norreel, B. (1999). Effects of rice cystatin I expression in transgenic potato on Colorado potato beetle larvae. Plant Science, 140(1), 71–79. https://doi.org/10.1016/S0168-9452(98)00197-6

Martin, P. A. W., Blackburn, M., Shropshire, A. D. S. (2006). Two new bacterial pathogens of Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 97(3), 774–780. https://doi.org/10.1603/0022-0493(2004)097[0774:tnbpoc]2.0.co;2

Martinez, M., Santamaria, M. E., Diaz-Mendoza, M., Arnaiz, A., Carrillo, L., Ortego, F. (2016). Phytocystatins: Defense proteins against phytophagous insects and acari. International Journal of Molecular Sciences, 17(10). MDPI AG. https://doi.org/10.3390/ijms17101747

Mi, X., Ji, X., Yang, J., Liang, L., Si, H., Wu, J., Zhang, N., Wang, D. (2015). Transgenic potato plants expressing cry3A gene confer resistance to Colorado potato beetle. Comptes Rendus - Biologies, 338(7), 443–450. https://doi.org/10.1016/j.crvi.2015.04.005

Michaud, D., Nguyen-Quoc, B., Yelle, S. (1993). Selective inhibition of Colorado potato beetle cathepsin H by oryzacystatins I and II. FEBS Letters, 331(1–2), 173–176. https://doi.org/10.1016/0014-5793(93)80320-T

Michiels, K., Van Damme, E. J. M., Smagghe, G. (2010). Plant-insect interactions: what can we learn from plant lectins? Archives of Insect Biochemistry and Physiology, 73(4), 193–212. https://doi.org/https://doi.org/10.1002/arch.20351

Muratoglu, H., Demirbag, Z., Sezen, K. (2011). The first investigation of the diversity of bacteria associated with Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Biologia, 66(2), 288–293. https://doi.org/10.2478/s11756-011-0021-6

Palma, L., Muñoz, D., Berry, C., Murillo, J., Caballero, P., Caballero, P. (2014). Bacillus thuringiensis toxins: An overview of their biocidal activity. Toxins, 6(12), 3296–3325). MDPI AG. https://doi.org/10.3390/toxins6123296

Panevska, A., Hodnik, V., Skočaj, M., Novak, M., Modic, Š., Pavlic, I., Podržaj, S., Zarić, M., Resnik, N., Maček, P., Veranič, P., Razinger, J., Sepčić, K. (2019). Pore-forming protein complexes from Pleurotus mushrooms kill western corn rootworm and Colorado potato beetle through targeting membrane ceramide phosphoethanolamine. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-41450-4

Panevska, A., Skočaj, M., Modic, Š., Razinger, J., Sepčić, K. (2020). Aegerolysins from the fungal genus Pleurotus – Bioinsecticidal proteins with multiple potential applications. Journal of Invertebrate Pathology, 107474. https://doi.org/10.1016/j.jip.2020.107474

Paul, S., Das, S. (2020). Natural insecticidal proteins, the promising bio-control compounds for future crop protection. The Nucleus. https://doi.org/10.1007/s13237-020-00316-1

Peumans, W. J., Van Damme, E. J. (1995). Lectins as plant defense proteins. Plant Physiology, 109(2), 347–352. https://doi.org/10.1104/pp.109.2.347

Pohleven, J., Brzin, J., Vrabec, L., Leonardi, A., Čokl, A., Štrukelj, B., Kos, J., Sabotič, J. (2011). Basidiomycete Clitocybe nebularis is rich in lectins with insecticidal activities. Applied Microbiology and Biotechnology, 91(4), 1141–1148. https://doi.org/10.1007/s00253-011-3236-0

Rane, A. S., Venkatesh, V., Joshi, R. S., Giri, A. P. (2020). Molecular investigation of Coleopteran specific α-amylase inhibitors from Amaranthaceae members. International Journal of Biological Macromolecules, 163, 1444–1450. https://doi.org/10.1016/j.ijbiomac.2020.07.219

Reed, G. L., Jensen, A. S., Riebe, J., Head, G., Duan, J. J. (2001). Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomologia Experimentalis et Applicata, 100(1), 89–100. https://doi.org/10.1046/j.1570-7458.2001.00851.x

Ryan, C. A. (1990). Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 28(1), 425–449.

https://doi.org/10.1146/annurev.py.28.090190.002233

Sabotič, J., Kos, J. (2012). Microbial and fungal protease inhibitors - Current and potential applications. Applied Microbiology and Biotechnology, 93(4), 1351–1375). https://doi.org/10.1007/s00253-011-3834-x

Sabotič, J., Ohm, R. A., Künzler, M. (2016). Entomotoxic and nematotoxic lectins and protease inhibitors from fungal fruiting bodies. Applied Microbiology and Biotechnology, 100(1), 91–111). https://doi.org/10.1007/s00253-015-7075-2

Schlüter, U., Benchabane, M., Munger, A., Kiggundu, A., Vorster, J., Goulet, M. C., Cloutier, C., Michaud, D. (2010). Recombinant protease inhibitors for herbivore pest control: A multitrophic perspective. Journal of Experimental Botany, 61(15), 4169–4183. https://doi.org/10.1093/jxb/erq166

Singh, S., Singh, A., Kumar, S., Mittal, P., Singh, I. K. (2020). Protease inhibitors: recent advancement in its usage as a potential biocontrol agent for insect pest management. Insect Science, 27(2), 186–201. https://doi.org/10.1111/1744-7917.12641

Šmid, I., Gruden, K., Buh Gašparič, M., Koruza, K., Petek, M., Pohleven, J., Brzin, J., Kos, J., Žel, J., Sabotič, J. (2013). Inhibition of the growth of Colorado potato beetle larvae by macrocypins, protease inhibitors from the parasol mushroom. Journal of Agricultural and Food Chemistry, 61(51), 12499–12509. https://doi.org/10.1021/jf403615f

Šmid, I., Rotter, A., Gruden, K., Brzin, J., Buh Gašparič, M., Kos, J., Žel, J., Sabotič, J. (2015). Clitocypin, a fungal cysteine protease inhibitor, exerts its insecticidal effect on Colorado potato beetle larvae by inhibiting their digestive cysteine proteases. Pesticide Biochemistry and Physiology, 122, 59–66. https://doi.org/10.1016/j.pestbp.2014.12.022

Srp, J., Nussbaumerová, M., Horn, M., Mareš, M. (2016). Digestive proteolysis in the Colorado potato beetle, Leptinotarsa decemlineata: Activity-based profiling and imaging of a multipeptidase network. Insect Biochemistry and Molecular Biology, 78, 1–11. https://doi.org/10.1016/j.ibmb.2016.08.004

Trdan, S. (2013). Insecticides - Development of safer and more effective technologies. V Insecticides - Development of Safer and More Effective Technologies. InTech. https://doi.org/10.5772/3356

Trdan, S. (2016). Insecticides Resistance. V Insecticides Resistance. InTech. https://doi.org/10.5772/60478

Tripathi, A. K., Mishra, S. (2016). Biotechnological Approaches. V Ecofriendly Pest Management for Food Security (str. 685–701). Elsevier Inc. https://doi.org/10.1016/B978-0-12-803265-7.00022-1

USEPA. (2010). BIOPESTICIDES REGISTRATION ACTION DOCUMENT. Bacillus thuringiensis Cry3Bb1 Protein and the Genetic Material Necessary for Its Production in MON 863 and MON 88017 Corns. http://www.epa.gov/pesticides/biopesticides/pips/cry3bb1-brad.pdf

Vandenborre, G., Smagghe, G., Van Damme, E. J. M. (2011). Plant lectins as defense proteins against phytophagous insects. Phytochemistry, 72(13), 1538–1550).

https://doi.org/10.1016/j.phytochem.2011.02.024

Varrot, A., Basheer, S. M., Imberty, A. (2013). Fungal lectins: Structure, function and potential applications. Current Opinion in Structural Biology, 23(5), 678–685). https://doi.org/10.1016/j.sbi.2013.07.007

Visal, S., Taylor, M. A. J., Michaud, D. (1998). The proregion of papaya proteinase IV inhibits Colorado potato beetle digestive cysteine proteinases. FEBS Letters, 434(3), 401–405.

https://doi.org/10.1016/S0014-5793(98)01018-7

Walski, T., Van Damme, E. J. M., Smagghe, G. (2014). Penetration through the peritrophic matrix is a key to lectin toxicity against Tribolium castaneum. Journal of Insect Physiology, 70, 94–101. https://doi.org/10.1016/j.jinsphys.2014.09.004

Wang, K., Shu, C., Zhang, J. (2019). Effective bacterial insecticidal proteins against coleopteran pests: A review. Archives of Insect Biochemistry and Physiology, 102(3), e21558. https://doi.org/https://doi.org/10.1002/arch.21558

Wang, M., Triguéros, V., Paquereau, L., Chavant, L., Fournier, D. (2002). Proteins as active compounds involved in insecticidal activity of mushroom fruitbodies. Journal of economic entomology, 95(3), 603–607. https://doi.org/10.1603/0022-0493-95.3.603

Wang, W., Hause, B., Peumans, W. J., Smagghe, G., Mackie, A., Fraser, R., Van Damme, E. J. M. (2003). The Tn antigen-specific lectin from ground ivy is an insecticidal protein with an unusual physiology. Plant Physiology, 132(3), 1322–1334. https://doi.org/10.1104/pp.103.023853

Whalon, M. E., Miller, D. L., Hollingworth, R. M., Grafius, E. J., Miller, J. R. (1993). Selection of a Colorado potato beetle (Coleoptera: Chrysomelidae) strain resistant to Bacillus thuringiensis. Journal of Economic Entomology, 86(2), 226–233. https://doi.org/10.1093/jee/86.2.226

Wolfson, J. L., Murdock, L. L. (1987). Suppression of larval Colorado potato beetle growth and development by digestive proteinase inhibitors. Entomologia Experimentalis et Applicata, 44(3), 235–240. https://doi.org/10.1111/j.1570-7458.1987.tb00550.x

Zhu, K., Huesing, J. E., Shade, R. E., Bressan, R. A., Hasegawa, P. M., Murdock, L. L. (1996). An insecticidal N-acetylglucosamine-specific lectin gene from Griffonia simplicifolia (Leguminosae). Plant Physiology, 110(1), 195 LP – 202. https://doi.org/10.1104/pp.110.1.195

Published

10. 11. 2021

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Review Article

How to Cite

ŽIGON, P., RAZINGER, J., & TRDAN, S. (2021). Insecticidal proteins and their potential use for Colorado potato beetle (Leptinotarsa decemlineata [Say, 1824]) control. Acta Agriculturae Slovenica, 117(3), 1–10. https://doi.org/10.14720/aas.2021.117.3.2221

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