The first-ever in-Russia discoveries of the entomopathogenic fungus Akanthomyces uredinophilus from the Republic of Adygea
- Авторлар: Cherepanova M.A.1, Mitina G.V.1, Choglokova A.A.1, Borisov B.A.2
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Мекемелер:
- All-Russian Institute of Plant Protection
- AgroBioTechnology LLC
- Шығарылым: Том 59, № 1 (2025)
- Беттер: 74-87
- Бөлім: PHYTOPATHOGENIC FUNGI
- URL: https://gynecology.orscience.ru/0026-3648/article/view/681169
- DOI: https://doi.org/10.31857/S0026364825010091
- EDN: https://elibrary.ru/srjnio
- ID: 681169
Дәйексөз келтіру
Аннотация
The first finding of cryptic entomopathogenic fungus Akanthomyces uredinophilus (Ascomycota, Hypocreales, Cordycipitaceae) in Russia is reported. Specimens were found in 2019 and 2022 in the North Caucasus at two 60 km distant points in the Republic of Adygea (1st – southern outskirts of Maykop, wooded damp ravine, N44°34ʹ24ʺ E40°08ʹ54ʺ, 240 m a. s. l.; 2nd – vicinity of Nickel settlement, Syuk River gorge, N44°10ʹ46ʺ E40°09ʹ29ʺ, 570 m a. s. l.) on dead insects: alien North American species of сitrus flatid planthopper Metcalfa pruinosa (Hemiptera, Auchenorrhyncha, Flatidae), whitefly Aleyrodes lonicerae (Hemiptera, Aleyrodidae), psyllid (Hemiptera, Psylloidea), and cranefly (Diptera, Tipuloidea). We have demonstrated high morphological and genetic (five gene loci EF1A, RPB1, RPB2, LSU and SSU) similarity of Adygean isolates with the type strain KACC44082 (Republic of Korea) from uredinia of the rust fungus Pucciniastrum agrimoniae and other isolates of Akanthomyces uredinophilus previously found in China and Argentina on dead insects. Under laboratory conditions all four Adygean isolates showed high virulence against larvae of population of green peach aphid Myzus persicae (Hemiptera, Aphididae) feeding on Vicia faba under experimental conditions including 25 ± 1°C temperature and spraying suspension with a spores (conidia) concentration 107 per 1 ml aphid mortality ranged from 30% [isolate MPi-Ad(Mp)19→Ak6] to 89% (isolate HPs – Ad22→B10) after three days. After seven days the mortality reached 100% in all variants, while it was only 15% in the control sample. This indicates the expediency of further study of these isolates as potential producers of commercial mycoinsecticides against harmful phytophagous insects.
Толық мәтін

Авторлар туралы
M. Cherepanova
All-Russian Institute of Plant Protection
Хат алмасуға жауапты Автор.
Email: cherepma@mail.ru
Ресей, Saint Petersburg, 196608
G. Mitina
All-Russian Institute of Plant Protection
Email: galmit@rambler.ru
Ресей, Saint Petersburg, 196608
A. Choglokova
All-Russian Institute of Plant Protection
Email: 4oglik@inbox.ru
Ресей, Saint Petersburg, 196608
B. Borisov
AgroBioTechnology LLC
Email: borborisov@mail.ru
Ресей, Moscow, 125212
Әдебиет тізімі
- Akhatov A.K., Izhevsky S.S., Meshkov Yu.I. et al. Pests of greenhouse and hothouse crops (morphology, lifestyle, harmfulness, control). Moscow, Partnership of Scientific Publications KMK, 2004. (In Russ.)
- Allen D.J. Verticillium lecanii on the bean rust fungus Uromyces appendiculatus. Trans. Br. Mycol. Soc. 1982. V. 79. P. 362–364.
- Askary H., Yarmand H. Development of the entomopathogenic hyphomycete Lecanicillium muscarium (Hyphomycetes: Moniliales) on various hosts. Eur. J. Entomol. 2007. V. 104. P. 67–72.
- Barson G. Laboratory studies on the fungus Verticillium lecanii, a larval pathogen of the large elm bark beetle (Scolytus scolytus). Ann. Appl. Biol. 1976. V. 83 (2). P. 207–214.
- Borisov B.A. Problems of development and using mycoinsecticidal formulations. In: Study of entomopathogenic microorganisms and development of technologies for their production and application. Romania, Bucharest, Research Institute of Plant Protection, 1990. P. 8–22. (In Russ.)
- Borisov B.A. Zooparasitic cordycipitoid fungi of the Sochi National Park and adjacent territories. In: Proceedings of the International Conference “Biodiversity and Ecology of Fungi and fungus-like Organisms in Northern Europe”. Ekaterinburg, 2015, pp. 31–35. (In Russ.)
- Borisov B.A. Discovery of tropical fungal parasites of arthropods Conoideocrella luteorostrata and Cordyceps thaxteri in the Moscow region – new examples of biota response to climate warming? In: Modern mycology in Russia. V. 6. Proceedings of the 4th Congress of Mycologists of Russia. Moscow, 2017, pp. 363–365. (In Russ.)
- Borisov B.A., Shoshina Ye.I., Karpun N.N. Entomoparasitic fungi as potential biological control agents of the adventive polyphagous pest Metcalfa pruinosa (Say) (Hemiptera: Auchenorrhyncha: Flatidae). In: Monitoring and biological methods for controlling pests and pathogens of woody plants: from theory to practice. Proceedings of the 3rd World Conference with International Participation. SIF SB RAS, Moscow, Krasnoyarsk, 2022. P. 30–31. (In Russ.)
- Chandler D., Davidson G., Jacobson R.J. Laboratory and glasshouse evaluation of entomopathogenic fungi against the two‐spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), on tomato, Lycopersicon esculentum. Biocontrol Sci. Technol. 2005. V. 15. P. 37–54. https://doi.org/10.1080/09583150410001720617
- Chen W.H., Han Y.F., Liang J.D. et al. Akanthomyces lepidopterorum, a new Lecanicillium-like species. Phytotaxa. 2020. V. 459 (2). P. 117–123. https://doi.org/10.11646/phytotaxa.459.2.3
- Cherepanova M.A., Choglokova A.A., Borisov B.A. et al. Polymorphism of Lecanicillium and Akanthomyces (Ascomycota, Hypocreales, Cordycipitaceae) fungi isolated from insects and rust fungi. In: Mechanisms of microorganism adaptation to various living conditions: papers for the 2nd World Scientific Conference with International Participation. Irkutsk, 28.02–06.03.2022. Irkutsk, 2022, pp. 180–181. (In Russ.)
- Ekbom B. Investigations on the potential of a parasitic fungus (Verticillium lecanii) for biological control of the greenhouse whitefly (Trialeurodes vaporariorum). Swed. J. Agr. Res. 1979. V. 9 (4). P. 129–138.
- Evlakhova A.A. Experiments on the control of citrus scale insects using the Сephalosporium fungus. In: Results of research work at VIZR for 1936, pt 3. Leningrad, 1938. P. 75–77. (In Russ.)
- Gams W. Cephalosporium-artige Schimmelpilze (Hyphomycetes). Stuttgart, G. Fischer Vertlag, 1971.
- Hall R.A. The fungus Verticillium lecanii as a microbial insecticide against aphids and scales. In: H.D. Burges (ed.). Microbial control of pests and plant diseases. Academic Press, L., 1981, pp. 483–498.
- Hall R.A. Control of whitefly Trialeurodes vaporariorum and cotton aphid Aphis gossypii in glasshouses by two isolates of the fungus Verticillium lecanii. Ann. Appl. Biol. 1982. V. 101. P. 1–11.
- Hall T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999. V. 41. P. 95–98.
- Hänssler G., Hermanns M. Verticillium lecanii as a parasite on cysts of Heterodera schachtii. Z. Pflanzenkrnkh. 1981. Bd. 88 (11). P. 678–681.
- Hänssler G., Knorzer M., Reisener H.-J. Lichtmicroskopische Untersuchungen der Interaction zwischen Puccinia graminis var. tritici und Verticillium lecanii. Phytopathol. Z. 1981. Bd 102 (3–4). P. 310–319.
- Hawksworth D.L. Introducing the draft BioCode. Bionomina. 2011. V. 3(1). P. 24–25.
- Huang B., Wang S., Fan M. et al. Two species of Akanthomyces from Dabieshan mountains. Mycosystema. 2000. V. 19. P. 172–174.
- Huson D.H., Scornavacca C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 2012. V. 61 (6). P. 1061–1067. https://doi.org/10.1093/sysbio/sys062
- Index Fungorum. CABI Bioscience, 2023. http://www.indexfungorum.org. Accessed 13.05.2024.
- Katoh K., Rozewicki J., Yamada K.D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinformatics. 2019. V. 20 (4). P. 1160–1166. https://doi.org/10.1093/bib/bbx108
- Kepler R.M., Luangsa-Ard J.J., Hywel-Jones N.L. et al. Phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus. 2017. V. 8 (2). P. 335–353. https://doi.org/10.5598/imafungus.2017.08.02.08
- Kim J.J., Goettel M.S., Gillespie D.R. Evaluation of Lecanicillium longisporum, Vertalec for simultaneous suppression of cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea, on potted cucumbers. Biol. Control. 2008, V. 45. P. 404–409. 10.1016/j.biocontrol.2008.02.003' target='_blank'>https://doi: 10.1016/j.biocontrol.2008.02.003
- Khonsanit A., Thanakitpipattana D., Mongkolsamrit S. et al. A phylogenetic assessment of Akanthomyces sensu lato in Cordycipitaceae (Hypocreales, Sordariomycetes): introduction of new genera, and the resurrection of Lecanicillium. Fungal Systematics and Evolution. 2024. V. 14. P. 271–305. https://doi: 10.3114/fuse.2024.14.17
- Liu Y.J., Whelen S., Hall B.D. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biol. Evol. 1999. V. 16 (12). P. 1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
- Malysh J., Kononchuk A., Frolov A. Detection of microsporidia infecting beet webworm Loxostege sticticalis (Pyraloidea: Crambidae) in European and Asian parts of Russia in 2006–2008. Plant Protection News. 2019. V. 2. P. 45–51. https://doi.org/10.31993/2308-6459-2019-2(100)-45-51
- Manfrino R., Gutierrez A., Diez del Valle F. et al. First description of Akanthomyces uredinophilus comb. nov. from hemipteran insects in America. Diversity. 2022. V. 14. Art. 1118. https://doi.org/10.3390/d14121118
- Mendgen K. Grown of Verticillium lecanii in pustules of stipe rust (Puccinia striiformis). Phytopathol. Z. 1981. Bd 102 (3–4). P. 301–309.
- Mendgen K., Casper R. Detection of Verticillium lecanii in pustules of bean rust (Uromyces phaseoli) by immunofluorescence. Phytopathol. Z. 1980. Bd 99 (4). P. 362–364.
- Meng Y., Wellabada Hewage Don P.I.D., Wang D. A new strain of Lecanicillium uredinophilum isolated from Tibetan Plateau and its insecticidal activity. Microorganisms. 2022. V. 10 (9). Art. 1832. https://doi: 10.3390/microorganisms10091832
- Meyer S.L.F. Evaluation of Verticillium lecanii strains applied in root drenches for suppression of Meloidogyne incognita on tomato. J. Helminthol. Soc. Wash. 1998. V. 65. P. 82–86.
- Meyer S.L.F., Wergin W.P. Colonization of soybean cyst nematode females, cysts and egg masses by the fungus Verticillium lecanii. J. Nematol. 1998. V. 30. P. 436–450.
- Miller T.C., Gubler W.D. Field application of Verticillium lecanii controls Sphaerotheca macularis f. sp. fragariae in California strawberry fruit pathogen. Phytopathol. 1988. V. 88. P. 63.
- Mitina G.V., Stepanycheva E.A., Choglokova A.A. et al. Features of behavioral reactions of the peach aphid Myzus persicae (Sulzer, 1776) (Hemiptera, Aphididae) to volatile organic compounds of entomopathogenic fungi of the genus Lecanicillium. Entmol. Rev. 2021. V. 101. P. 1015–1023. https://doi.org/10.1134/S0013873821080017
- Mitina G.V., Tokarev Yu.S., Kazartsev I.A. et al. The molecular genetic characteristics of the entomopathogenic fungal strains from the genus Lecanicillium (= Verticillium lecanii s.l.). Mikologiya i fitopatologiya. 2015. V. 49 (2). P. 109– 115. (In Russ.)
- Mongkolsamrit S., Noisripoom W., Tasanathai K. et al. Comprehensive treatise of Hevansia and three new genera Jenniferia, Parahevansia and Polystromomyces on spiders in Cordycipitaceae from Thailand. MycoKeys. 2022. V. 91. P. 113–149. https://doi.org/10.3897/ mycokeys.91.83091
- Nikitsky N.В., Bibin А.R., Dolgin М.М. Xylophilous beetles (Coleoptera) of the Caucasian State Biospheric Natural Reserve and adjacent territories. Institute of Biology of Komi centre of science, Ural branch of the RAS, Siktivkar, 2008. (In Russ.)
- Park M.J., Hong S.B., Shin H.D. Lecanicillium uredinophilum sp. nov. associated with rust fungi from Korea. Mycotaxon. 2015. V. 130. P. 997–1005. https://doi.org/10.5248/130.997
- Rehner S.A., Buckley E. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia. 2005. V. 97(1). P. 84–98. https://doi.org/10.3852/mycologia.97.1.84
- Rehner S.A., Minnis A.M., Sung G.H. et al. Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia. 2011. V. 103 (5). P. 1055–1073. https://doi: 10.3852/10–302
- Shrestha B., Kubátová A., Tanaka E. et al. Spider-pathogenic fungi within Hypocreales (Ascomycota): Their current nomenclature, diversity, and distribution. Mycol. Progress. 2019. V. 18 (8). P. 983–1003. https://doi.org/10.1007/s11557-019-01512-3
- Solovey E.F. Heterogeneity of populations of the fungus Verticillium lecanii Viegas. Mikologiya i fitopatologiya. 1980. V. 14 (5). P. 400–404.
- Steenberg T., Humber R.A. Entomopathogenic potential of Verticillium and Acremonium species (Deuteromycotina: Hyphomycetes). J. Invertebr. Pathol. 1999. V. 73. P. 309–314.
- Stiller J.W., Hall B.D. The origin of red algae: implications for plastid evolution. Proc. Nat. Acad. Sci. 1997. V. 94 (9). P. 4520–4525. https://doi.org/10.1073/pnas.94.9.4520
- Sung G.H., Hywel-Jones N.L., Sung J.M. et al. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud. Mycol. 2007. V. 57. P. 5–59. https://doi: 10.3114/sim.2007.57.01
- Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis v. 11. Mol. Biol. Evol. 2021. V. 38 (7). P. 3022–3027. https://doi.org/10.1093/molbev/msab120
- Viegas A. Un amigo do fazendeiro Verticillium lecanii (Zimm.) n. comb., o cansador do halo brauco do Coccus viridis Green. Rev. Inst. Café Estado Saõ Paulo. 1939. V. 14. P. 754–772.
- Vilgalys R., Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 1990. V. 172 (8). P. 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
- Wang Y.B., Wang Y., Fan Q. et al. Multigene phylogeny of the family Cordycipitaceae (Hypocreales): new taxa and the new systematic position of the Chinese cordycipitoid fungus Paecilomyces hepiali. Fungal Diversity. 2020. V. 103. P. 1–46. https://doi.org/10.1007/s13225-020-00457-3
- Wang Y., Wang Z.Q., Luo R. et al. Species diversity and major host/substrate associations of the genus Akanthomyces (Hypocreales, Cordycipitaceae). MycoKeys. 2024. V. 101. P. 113–141.
- https://doi.org/10.3897/mycokeys.101.109751
- Wei D.P., Wanasinghe D.N., Chaiwat T.A. et al. Lecanicillium uredinophilum known from rusts, also occurs on animal hosts with chitinous bodies. Asian J. Mycol. 2018. V. 1 (1). P. 63–73. https://doi.org/10.5943/ajom/1/1/5
- White T.J., Bruns T.D., Lee S.B. et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. 1990. V. 18 (1). P. 315–322.
- Zare R., Gams W. A revision of Verticillium sect. Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia. 2001. V. 73 (1–2). P. 1–50. https://doi.org/10.1127/nova.hedwigia/71/2001/1
- Zare R., Gams W. A revision of Verticillium sect. Prostrata. 1V. The genus Haptocillium. Nova Hedwigia. 2001a. V. 73 (3– 4). P. 271–292. https://doi.org/10.1127/nova.hedwigia/73/2001/271
- Zare R., Gams W., Culham A. A revision of Verticillium sect. Prostrata. 1. Phylogenetic studies using ITS sequeces. Nova Hedwigia. 2000. V. 71 (3–4). P. 465–480. https://doi.org/10.1127/nova/71/2000/465
- Zare R., Gams W., Evans H.C. A revision of Verticillium sect. Prostrata. V. The genus Pochonia, with notes on Rotiferospora. Nova Hedwigia. 2001. V. 73 (1–2). P. 51–86. https://doi.org/10.1127/nova.hedwigia/73/2001/51
- Zhang Z.F., Zhou S.Y., Eurwilaichitr L. et al. Culturable mycobiota from Karst caves in China II, with descriptions of 33 new species. Fungal Diversity. 2020. https://doi.org/10.1007/s13225-020-00453-7
- Ахатов А.К., Ижевский С.С., Мешков Ю.И. и др. (Akhatov et al.) Вредители тепличных и оранжерейных растений (морфология, образ жизни, вредоносность, борьба). Москва: Товарищество научных изданий КМК, 2004. 307 с.
- Борисов Б.А. (Borisov) Проблемы создания и использования микоинсектицидных препаратов // Изучение энтомопатогенных микроорганизмов и разработка технологий их производства и применения. Румыния, Бухарест: НИИ защиты растений, 1990. С. 8–22.
- Борисов Б.А. (Borisov) Зоопаразитические кордиципитоидные грибы Сочинского национального парка и прилегающих территорий // Биоразнообразие и экология грибов и грибоподобных организмов Северной Евразии: Матер. Всеросс. конфер., Екатеринбург, 20–24 апреля 2015 г. Екатеринбург: Изд-во Уральского ун-та, 2015. С. 31–35.
- Борисов Б.А. (Borisov) Обнаружение тропических грибов – паразитов членистоногих Conoideocrella luteorostrata и Cordyceps thaxteri в Московской области – новые примеры отклика биоты на потепление климата? // Современная микология в России. Т. 6. Материалы 4-го съезда микологов России. Москва: Национальная академия микологии, 2017. С. 363–365.
- Борисов Б.А., Шошина Е.И., Карпун Н.Н. (Borisov et al.) Энтомопаразитические грибы как потенциальные агенты биологического контроля адвентивного многоядного вредителя – белой цикадки Metcalfa pruinosa (Say) (Hemiptera: Auchenorrhyncha: Flatidae) // Мониторинг и биологические методы контроля вредителей и патогенов древесных растений: от теории к практике. Матер. 3 всеросс. конфер. Москва, 11–15 апреля 2022 г. Москва; Красноярск: ИЛ СО РАН, 2022. С. 30–31.
- Евлахова А.А. (Evlakhova) Опыты по борьбе с цитрусовыми червецами посредством гриба цефалоспориум // Итоги научно-исследовательских работ ВИЗР за 1936 г., ч. 3. Л., 1938. С. 75–77.
- Митина Г.В., Токарев Ю.С., Казарцев И.А. и др. (Mitina et al.) Молекулярно-генетическая характеристика штаммов энтомопатогенных грибов рода Lecanicillium (= Verticillium lecanii s.l.) // Микология и фитопатология. 2015. Т. 49 (2). С. 109–115.
- Никитский Н.Б., Бибин А.Р., Долгин М.М. (Nikitsky et al.) Ксилофильные жесткокрылые (Coleoptera) Кавказского государственного природного биосферного заповедника и сопредельных территорий. Сыктывкар: Институт биологии Коми НЦ УРО РАН, 2008. 452 с.
- Черепанова М.А., Чоглокова А.А., Борисов Б.А. и др. (Cherepanova et al.) Полиморфизм грибов Lecanicillium и Akanthomyces (Ascomycota, Hypocreales, Cordycipitaceae), выделенных из насекомых и ржавчинных грибов // Механизмы адаптации микроорганизмов к различным условиям среды обитания: тезисы докладов 2 всеросс. научной конференции с международным участием. Иркутск, 28 февраля – 6 марта 2022 г. Иркутск: Изд-во ИГУ, 2022. С. 180–181.
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