Characterization of Parastagonospora nodorum and Parastagonospora pseudonodorum populations in the Russian Federation based on the presence of effector genes
https://doi.org/10.30766/2072-9081.2026.27.4.850-866
Abstract
The objective of this study was to evaluate populations of the fungi Parastagonospora nodorum and P. pseu-donodorum from the Leningrad, Tambov, and Amur regions of the Russian Federation for the presence of the effector genes SnToxA, SnTox1, SnTox3, SnTox5, and SnTox267. Leaf samples showing symptoms of septoria were collected in 2025 from various spring wheat cultivars at the milk-wax ripeness stage of grain. The investigations were carried out using light micros-copy, PCR, and CTAB methods. Screening of 165 P. nodorum isolates and 19 P. pseudonodorum isolates revealed significant inter- and intraspecific differences in the distribution of effector genes. It was established that SnTox3 had the highest preva-lence among P. nodorum genotypes (53 %), whereas the distribution of SnTox5 was strictly linked to the geographic origin of the samples (European part of Russia – up to 100 %; Amur region – 0 %). Isolates of P. pseudonodorum from the Tambov region were characterized by the presence of SnToxA (79 %), SnTox3 (79 %), and SnTox5 (100 %), while SnTox267 occurred less frequently (58 %), and SnTox1 was absent. Upon summarization of the data obtained from a five-year monitoring (2021–2025) of P. nodorum and P. pseudonodorum populations from different regions of the Russian Federation, a high het-erogeneity in the distribution of the necrotrophic effector genes SnToxA, SnTox1, SnTox3, SnTox267, and SnTox5 was revealed. Species-specific and geographic differentiation in gene occurrence frequencies, as well as their temporal dynamics, were established. The research presents for the first time the results of applying the primer pair SnTox5_qPCR_F/ SnTox5_qPCR_R for testing Russian populations of Parastagonospora spp. for the presence of the SnTox5 gene. As part of the initiated work on studying the species composition of wheat septoria pathogens from the Blagoveshchensk district of the Amur region, P. nodorum was identified as the predominant species in the phytopathogenic complex.
Keywords
About the Authors
Yu. V. ZelenevaRussian Federation
Yuliуa V. Zeleneva, DSc in Biology, associate professor, senior researcher, the Laboratory of Mycology and Phyto-pathology
Podbelskogo shosse, 3, St. Petersburg, Pushkin, 196608
T. P. Kolesnikova
Russian Federation
Tatyana P. Kolesnikova, PhD in Biology, leading researcher, the Laboratory of Plant Protection
86 Politekhnicheskaya Street, Blagoveshchensk, Amur Region, 675000
N. M. Terexin
Russian Federation
Nikolaj M. Terexin, Junior Researcher, the Laboratory of Grain Crop Breeding
86 Politekhnicheskaya Street, Blagoveshchensk, Amur Region, 675000
V. P. Sudnikova
Russian Federation
Valentina P. Sudnikova, PhD in Agricultural Science, senior researcher, the Laboratory of Plant Immunity
30 Michurin street, Michurinsk, Tambov region, 393774
M. V. Ryabova
Russian Federation
Mariya V. Ryabova, 2nd-year Master's student, Institute of Engineering and Technology
33 Internatcionalnaya street, Tambov, 92000
References
1. Fones H., Gurr S. The impact of Septoria tritici blotch disease on wheat: An EU perspective. Fungal Genetics and Biology. 2015;79:3–7. DOI: https://doi.org/10.1016/j.fgb.2015.04.004
2. Birr T., Hasler M., Verreet J-A., Klink H. Temporal Changes in Sensitivity of Zymoseptoria tritici Field Populations to Different Fungicidal Modes of Action. Agriculture. 2021;11(3):269.DOI: https://doi.org/10.3390/agriculture11030269
3. Petit-Houdenot Y., Lebrun M. H., Scalliet G. Understanding plant-pathogen interactions in Septoria tritici blotch infection of cereals. In: Achieving durable disease resistance in cereals. London, UK: Burleigh Dodds Science Publishing. 2021:263–302. DOI: https://doi.org/10.1201/9781003180715-11
4. Zeleneva Yu. V., Ablova I. B., Sudnikova V. P., Mokhova L. M., Konkova E. A. Species composition of wheat septoria pathogens in the european part of Russia and identifying SnToxA, SnTox1, and SnTox3 effector genes. Mikologiya i fitopatologiya = Mycology and Phytopathology. 2022;56(6):441–447. (In Russ.). DOI: https://doi.org/10.31857/S0026364822060113
5. Zeleneva Yu. V., Gannibal F. B., Kazartsev I. A., Sudnikova V. P. Molecular identification, effector genes and virulence of isolates of Parastagonospora nodorum from Altai krai (Russia). Mikologiya i fitopatologiya = Mycology and Phytopathology. 2023;57(5):362–371. (In Russ.). DOI: https://doi.org/10.31857/S0026364823050124
6. Zhelezova S. V., Pakholkova E. V., Veller V. E., Voronov M. A., Stepanova E. V., Zhelezova A. D. et al. Hyperspectral Non-Imaging Measurements and Perceptron Neural Network for Pre-Harvesting Assessment of Damage Degree Caused by Septoria/Stagonospora Blotch Diseases of Wheat. Agronomy. 2023;13(4):1045. DOI: https://doi.org/10.3390/agronomy13041045
7. Ficke A., Cowger C., Bergstrom G., Brodal G. Understanding yield loss and pathogen biology to improve disease management: Septoria nodorum blotch – a case study in wheat. Plant Disease. 2018;102(4):696–707. DOI: https://doi.org/10.1094/PDIS-09-17-1375-FE
8. Haugrud A. R. P., Zhang Z., Friesen T. L., Faris J. D. Genetics of resistance to Septoria nodorum blotch in wheat. Theoretical and Applied Genetics. 2022;135(11):3685–3707. DOI: https://doi.org/10.1007/s00122-022-04036-9
9. Kariyawasam G. K., Nelson A. C., Williams S. J., Solomon P. S., Faris J. D., Friesen T. L. The Necrotrophic Pathogen Parastagonospora nodorum Is a Master Manipulator of Wheat Defense. Molecular Plant-Microbe Interactions. 2023;36(12):764–773. DOI: https://doi.org/10.1094/MPMI-05-23-0067-IRW
10. Navathe S., Yadav P. S., Chand R., Mishra V. K., Vasistha N. K., Meher P. K. et al. ToxA–Tsn1 interaction for spot blotch susceptibility in Indian wheat: an example of inverse genefor-gene relationship Plant Disease. 2020;104(1):71–81. DOI: https://doi.org/10.1094/PDIS-05-19-1066-RE
11. Faris J. D., Friesen T. L. Plant genes hijacked by necrotrophic fungal pathogens. Current Opinion in Plant Biology. 2020;56:74–80. DOI: https://doi.org/10.1016/j.pbi.2020.04.003
12. Friesen T. L., Faris J. D. Characterization of effector–target interactions in necrotrophic pathosystems reveals trends and variation in host manipulation. Annual Review of Phytopathology. 2021;59:77–98. DOI: https://doi.org/10.1146/annurev-phyto-120320-012807
13. Zhang Z., Running K. L. D., Seneviratne S., Peters‐Haugrud A. R., Szabo‐Hever A., Shi G. et al. A protein kinase‐major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. The Plant Journal. 2021;106(3):720–732. DOI: https://doi.org/10.1111/tpj.15194
14. Richards J. K., Kariyawasam G. K., Seneviratne S., Wyatt N. A., Xu S. S., Liu Z. et al. A triple threat: the Parastagonospora nodorum SnTox267 effector exploits three distinct host genetic factors to cause disease in wheat. New Phytologist. 2022;233(1):427–442. DOI: https://doi.org/10.1111/nph.17601
15. Kolomiyets T. M., Pakholkova E. V., Dubovaya L. P. Selection of the starting material for the creation of wheat varieties with long-term resistance to septoria. Moscow: Pechatnyy gorod, 2017. 56 p.
16. Kazartsev I. A., Zeleneva Yu. V. Development and application of multiplex PCR for identification of three fungal species of the genus Parastagonospora widespread in Russia. Vestnik zashchity rasteniy = Plant Protection News. 2025;108(2):107–111. (In Russ.). DOI: https://doi.org/10.31993/2308-6459-2025-108-2-17138
17. Doyle J. J., Doyle J. L. Isolation of plant DNA from fresh tissue. Focus. 1990;12(1):13–15.
18. Andrie R. M., Pandelova I., Ciuffetti L. M. A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathology. 2007;97(6):694–701. DOI: https://doi.org/10.1094/PHYTO-97-6-0694
19. Gao Y., Faris J. D., Liu Z., Kim Y. M., Syme R. A., Oliver R. P. et al. Identification and characterization of the SnTox6‐Snn6 interaction in the Parastagonospora nodorum–wheat pathosystem. Molecular Plant–Microbe Interactions. 2015;28(5):615–625. DOI: https://doi.org/10.1094/MPMI-12-14-0396-R
20. Kariyawasam G. K., Richards J. K., Wyatt N. A., Running K. L. D., Xu S. S., Liu Z. et al. The Parastagonospora nodorum necrotrophic effector SnTox5 targets the wheat gene Snn5 and facilitates entry into the leaf mesophyll. New Phytologist. 2022;233(1):409–426. DOI: https://doi.org/10.1111/nph.17602
21. Kolesnikova T. P., Terekhin N. M., Zeleneva Yu. V., Kon’kova E. A., Kovalenko N. M. Juvenile resistance of wheat varieties and lines Developed by the far eastern SAU to leaf and stem diseases. Zernovoye khozyaystvo Rossii = Grain Economy of Russia. 2025;17(4):105–112. (In Russ.). DOI: https://doi.org/10.31367/2079-8725-2025-99-4-105-112
22. Zeleneva Yu. V., Konkova E. A. Soft wheat cultivars grown in the Saratov region and their resistance to septoria blotch. Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2023;27(6):582–590. (In Russ.). DOI: https://doi.org/10.18699/VJGB-23-70
23. Kovalenko N. M., Zeleneva Yu. V., Sudnikova V. P. Characterization of Pyrenophora tritici-repentis, Parastagonospora nodorum, and Parastagonospora pseudonodorum in the Tambov Oblast for the Presence of Effector Genes. Russian Agricultural Sciences. 2023;49(3):285–291. DOI: https://doi.org/10.3103/S1068367423030114
24. Zeleneva Yu. V., Sudnikova V. P., Gusev I. V., Baranova O. A. Identification of effector genes of Parastagonospora nodorum, P. pseudonodorum in tambov populations and sensitivity genes to NEs in varieties and hybrid lines of spring soft wheat. Ekologicheskaya genetika. 2024;22(2):139–150. (In Russ.). DOI: https://doi.org/10.17816/ecogen627323
25. Zeleneva Yu. V., Ablova I. B., Mokhova L. M. Species Composition of Wheat Septoria Pathogens and Identification of Effector Genes in Parastagonospora spp. populations of Krasnodar Krai and Leningrad Oblast of the Russian Federation. Russian Agricultural Sciences. 2024;50(4):383–390. DOI: https://doi.org/10.3103/S1068367424700393
Review
For citations:
Zeleneva Yu.V., Kolesnikova T.P., Terexin N.M., Sudnikova V.P., Ryabova M.V. Characterization of Parastagonospora nodorum and Parastagonospora pseudonodorum populations in the Russian Federation based on the presence of effector genes. Agricultural Science Euro-North-East. 2026;27(4):850-866. (In Russ.) https://doi.org/10.30766/2072-9081.2026.27.4.850-866
JATS XML






























