Significance of the works of E.V. Talalaev in the formulation of a development strategy for biotechnological pest management methods

The development of methods for pest management continued to be one of the main directions in development of biotechnology throughout the twentieth century. In Russia, the development of this research area is inextricably linked with the name of Evgeny V. Talalayev, professor of Irkutsk State University and the founder of the biological forest protection approach. Though his enterprise, theoretical foundations for the use of the microbiomethod were developed, along with the first domestic bacterial preparation against the Siberian silkworm, dendrobacillin. Large-scale tests of the preparation were carried out to demonstrate its safety in terms of human health. With his direct participation, industrial production of biological products was organised in the USSR. These products were in great demand in both domestic and foreign markets. The article gives a brief history of the study of the entomopathogenic properties of Bacillus Thuringiensis and the development of biotechnological methods for pest management on its basis. A brief comparative analysis is provided for the current state of microbiomethods for the protection of plant species in Russia and abroad. The results of the first decades of large-scale application in agricultural production based on B. thuringiensis genetic engineering Bt-technologies, positioned as a more effective and economical alternative to the microbiome, are considered. The main reasons for the low efficiency of this area of plant genetic engineering as described in the scientific literature are presented. Additionally, the problem of discounting the development patterns of natural parasitic systems underlying the microbiomethod during the creation of transgenic BT plants is considered. An assessment for the value of the scientific heritage of E.V. Talalayev for the development of plant protection methods based on B. Thuringiensis is made along with the presentation of a number of new directions for the development of plant biotechnologies on their basis. Further prospects for the use of the microbiomethod plant protection approach in the Russian Federation are discussed.

The authors declare no conflict of interests regarding the publication of this article.

1. Shternshis MV. Trends of microbial pesticides biotechnology developed for plant protection in Russia. Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya = Tomsk State University Journal of Biology. 2012;2(18):92–100. (In Russian)

2. Ishiwata S. On a kind of severe flacherie (sotto disease). Dainihon Sanshi Kaiho. 1901; 114:(1–5).

3. Berliner E. Über die Schlaffsucht der Mehlmottenraupe. Zeitschrift für das gesamte Getreidewesen. 1911;3:63–70. (In German)

4. Berliner E. Über die Schlaffsucht der Mehlmottenraupe (Ephestia kühniella Zell.) und ihren Erreger Bacillus thuringiensis n. sp. Zeitschrift für Angewandte Entomologie. 1915;2(1):29–56. (In German). https://doi.org/10.1111/j.1439-0418.1915. tb00334.x

5. Sanchis V. From microbial sprays to insectresistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review. Agronomy for Sustainable Development. 2011;31(1):217–231.

6. Goldberg LJ, Margalit J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti and Culex pipiens. Mosquito News. 1977;37(3):355–358.

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

8. Angus TA. A bacterial toxin paralyzing silkworm larvae. Nature. 1954;173(4403):545–546. https://doi.org/10.1038/173545a0

9. Hannay CL. Crystalline inclusions in aerobic sporeforming bacteria. Nature. 1953;172(4387):1004. https://doi.org/10.1038/1721004a0

10. Hannay CL, Fitz-James P. The protein crystals of Bacillus thuringiensis Berliner. Canadian Journal of Microbiology. 1955;1(8):694–710. https://doi.org/ 10.1139/m55-083

11. Schnepf HE, Whiteley HR. Cloning and expression of the Bacillus thuringiensis crystal protein gene in Escherichia coli. Proceedings of the National Academy of Sciences USA. 1981;78(5):2893–2897. https://doi.org/10.1073/pnas.78.5.2893

12. BravoA,GomezI,Garcia-Gomez B, Jnofre J, Soberon M. Insecticidal proteins from Bacillus thuringiensis and their mechanism of action. In: Fiuza LM, Polanczyk RA, Crickmore N. (eds.) Bacillus thuringiensis and Lysinibacillus sphaericus. Springer International Publishing AG, 2017. P. 53–66. https://doi.org/10.1007/978-3-319-56678-8_4

13. Ibrahim MA, Griko N, Junker M, Bulla LA. Bacillus thuringiensis: A genomics and proteomics perspective. Bioengineered Bugs. 2010;1(1):31–50. https://doi.org/10.4161/bbug.1.1.10519

14. Sanahuja G, Banakar R, Twyman RM, Capell T, Christou B. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnology Journal. 2011;9(3):283–300. https://doi.org/10.1111/j.1467-7652.2011.00595.x

15. Bacillus thuringiensis Biotechnology. Sansinenea E. (ed.) Springer Science and Business Media; 2012. 392 p.

16. ISAAA Brief 54: Global Status of Commercialized Biotech/GM Crops: 2018. Biotech Crops Continue to Help Meet the Challenges of Increased Population and Climate Change. Available from: http://www.isaaa.org/resourses/publications/briefs/5 4/ executivesummary/pdf/B54-ExecSum-English.pdf [Accessed 20th October 2019].

17. Viktorov AG. Can efficient insecticidal plants be created or the evolution of phytophage resistance to commercial transgenic Bt-Plants. Russian JourNal of Plant Physiology. 2015;62(1):14–22. https://doi. org/10.1134/S102144371501015X

18. Viktorov AG. Current trends in the global market of transgenic plants and environmental safety issues. Russian Journal of Plant Physiology. 2016; 63(1):38–45. https://doi.org/10.1134/S1021443716010179

19. Talalaev EV. Bacteriological method of combating the Siberian silkworm. Irkutsk: Irkutskoe knizhnoe izdatel’stvo; 1961. 49 p. (In Russian)

20. Talalaev EV. To the question of the deve lopment of a microbiological method of controlling the Siberian silkworm (preliminary communication of 1951). Izvestiya Biologo-geograficheskogo nauchnoissledovatel'skogo instituta pri Irkutskom universitete. 1956;16(1-4):62–71. (In Russian)

21. BiryukovAD. Beneficial microbes. In: The history of industry in Novosibirsk. Vol. 5. New countdown (1986–2005). Novosibirsk: Izdatel'skii dom “Istoricheskoe nasledie Sibiri”; 2005. P. 435–482. (In Russian)

22. Talalaev EV. Essays on the development of a microbiological method to combat the siberian silkworm. Irkutsk: Irkutsk State University; 1991. 128 p. (In Russian)

23. Вeliakov VD. General regularities of functioning of parasitic systems (mechanisms of selfregulation). Parazitologiya. 1986;20(4):249–255. (In Russian)

24. Chaika SYu. Parasitism – an existence of organisms in a structure of parasitic systems. Parazitologiya. 1998;2(1):3–10. (In Russian)

25. Chaika SYu. Parasitism and parasitic systems. Veterinarnaya patologiya = Veterinary pathology. 2004;3:19–27. (In Russian)

26. TalalaevEV. Septicemia of caterpillars of the Siberian silkworm. Mikrobiologiya. 1956;25(1):99-102. (in Russian)

27. Tanada Y. Bacillus thuringiensis: integrated control – past, present and future. In: Cheng TC. (ed.) Pathogens of Invertebrates. Comparative Pathobiology. Springer, Boston: 1984;7:59–90.

28. Knipling EF. Edward Arthur Steinhaus (1914–1969). In: Biographical Memoirs. Washington: National Academy of Sciences. 1974;44:321–327.

29. Steinhaus EA. Possible use of Bacillus thuringiensis Berliner as an aid in the biological control of the alfalfa caterpillar. Hilgardia. 1951;20(8):359– 381. https://doi.org/10.3733/hilg.v20n18p359

30. Steinhaus EA. On the Improbability of Bacillus thuringiensis Berliner Mutating to Forms Pathogenic for Vertebrates. Journal of Economic Entomology. 1959;52(3):506–508. https://doi.org/10.1093/jee/52.3.506

31. Kuznetsov VV, Kulikov AM, Tsydendambaev VD. Genetically modified crops and products derived from them: food, environmental and agrotechnical risks. Izvestiya agrarnoi nauki. = Proceedings of agricultural sciences. 2010;8(3):10–31. (In Russian)

32. ChemerisAV, Bikbulatova SM, Chemeris DA, Baymiev AlK, Knyazev AV, Kuluev BR, et al. Should beware of the gmos? on-site observers view on the hysteria around. Biomika. = Biomics. 2014;6(2):77–138. (In Russian)

33. Viktorov AG.Ecological and physiological features of Bt-plants causing outbreaks of secondary pests. Russian Journal of Plant Physiology. 2017;64(4): 457–463. https://doi.org/10.1134/S1021443717040185

34. Burdon JJ, Thrall PH. Coevolution of plants and their pathogens in natural habitats. Science. 2009; 324(5928):755–756. https://doi.org/10.1126/science.1171663

35. Thrall PH, Hochberg ME, Burdon JJ, Bever JD. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology and Evolution. 2007;22(3):120–126.

36. Gandon S, Buckling A, Decaestecker E, DayT. Host–parasite coevolution and patterns of adaptation across time and space. Journal of evolutionary biology. 2008;21(6):1861–1866. https://doi.org/10.1111/j.1 420-9101.2008.01598.x

37. Wolinska J, King K.C. Environment can alter selection in host–parasite interactions. Trends in parasitology. 2009;25(5):236–244. https://doi.org/10.10 16/j.pt.2009.02.004

38. Enikeev AG. Transgenic Plants: New Biological System or New Properties of Plant-Agrobacterium Symbiosis? Russian Journal of Plant Physiology. 2018;65(5):621–627. https://doi.org/10.1134/S1 0 214 43718050060

39. Provorov NA, Vorobyov NI, Andronov EE. Macro- and microevolution of bacteria in symbiotic systems. Russian Journal of Genetics. 2008;44(1):6– 20. https://doi.org/10.1134/S102279540801002X

40. Bizyukova OV. World microbiological preparations market survey. Zashchita i karantin rastenii = Protection and quarantine of plants. 2012;3:9–12. (In Russian)

41. Valent Bio Sciences. Available from: https://www.valentbiosciences.com [Accessed 20th December 2018].

42. Shternshis MV, Belyaev AA, Cvetkova VP, Shpatova TV, Lelyak AA, Bahvalov SA. Biological products based on bacteria of the bacillus genus for plant health management. Novosibirsk: Publishing House of the SB RAS; 2016. 233 p. (In Russian)

43. Kamenek LK, Terekhina LD, Kamenek VM, Andreeva IV, Terekhin DA, Vorontsov VV. Study of the growth-promoting effect of delta-endotoxin on the example of cucumber plants. Vestnik Novosibirskogo gosudarstvennogo agrarnogo universiteta = Bulletin of Novosibirsk State Agrarian University. 2010;4: 13–17. (In Russian)

44. Basyrova LF, Kamenek DV, Kamenek LK, Terekhina LD. The effect of bacillus thuringiensis delta endotoxin on the biochemical composition of cucumber (cucumis sativus) fruits. Vestnik Altaiskogo gosudarstvennogo agrarnogo universiteta = Bulletin of Altai State Agricultural University. 2014;10:14–19. (In Russian)

45. Korobov YaA, Kamenek DV, Kamenek LK. Growth-promoting effect of Bacillus thuringiensis delta-endotoxin on juvenile plantsarsicum annuum. Vestnik Altaiskogo gosudarstvennogo agrarnogo universiteta = Bulletin of Altai State Agricultural University. 2014;11:14–19.

46. Korobov YaA, Kamenek DV, Kamenek LK, Useeva LF. Growth-stimulating effect of delta-endotoxin Bacillus thuringiensis on wheat during juvenile phase. Ul'yanovskii mediko-biologicheskii zhurnal. = Ulyanovsk Medico-Biological Journal. 2017;2:152–158. https://doi.org/10.23648/UMBJ.2017.26.6230

47. Ito A, Sasaguri Y, Kitada S, Kusaka Y, Kuwano K, Masutomi K, et al. A Bacillus thuringiensis Crystal Protein with Selective Cytocidal Action to Human Cell. Journal of Biological Chemistry. 2004; 279(20):21282–21286. https://doi.org/10.1074/jbc. M401881200

48. Kitada S, Abe Y, Shimada H, Kusaka Y, Matsuo Y, Katayama H, et al. Cytocidal actions of parasporin-2, an anti-tumor crystal toxin from Bacillus thuringiensis. Journal of Biological Chemistry. 2006; 281(36): 26350–26360. https://doi.org/10.1074/jbc. M602589200