agronaukaАграрная наука Евро-Северо-ВостокаAgricultural Science Euro-North-East2072-90812500-1396FARC North-East10.30766/2072-9081.2025.26.1.7-20agronauka-1874Research ArticleОБЗОРНЫЕ СТАТЬИREVIEWПрименение ДНК-маркеров в селекции пшеницы на устойчивость к пыльной головне (обзор)The use of DNA markers in wheat breeding for resistance to loose smut (review)https://orcid.org/0000-0002-0554-5814ХаринаА. В.KharinaAnastasia V.

Харина Анастасия Владимировна, кандидат с.-х. наук, научный сотрудник

ул. Ленина, 166 а, Киров, 610007

Anastasia V. Kharina, PhD in Agricultural Science, researcher

166-a Lenin str., Kirov, 610007

Khavchas@yandex.ruhttps://orcid.org/0000-0002-0638-4258НовоселоваН. В.NovoselovaNina V.

Новоселова Нина Владиславовна, младший научный сотрудник

ул. Ленина, 166 а, Киров, 610007

Nina V. Novoselova, junior researcher

166-a Lenin str., Kirov, 610007

priemnaya@fanc-sv.ruФГБНУ «Федеральный аграрный научный центр Северо-Востока имени Н.В. Рудницкого»РоссияFederal Agricultural Research Center of the North-East named N.V. RudnitskyRussian Federation202527022025261720Copyright © Харина А.В., Новоселова Н.В., 20252025Харина А.В., Новоселова Н.В.Kharina A.V., Novoselova N.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.agronauka-sv.ru/jour/article/view/1874

Пшеница (Triticum aestivum L.) является важной и востребованной культурой во всем мире. Значительное снижение ее урожайности обусловлено поражением болезнями, одно из наиболее опасных заболеваний – пыльная головня (Ustilago tritici (Pers.) Rostr.). Самый эффективный, экономически выгодный и экологически оправданный способ борьбы с болезнью – создание устойчивых сортов с применением молекулярно-биологических методов. В работе проанализированы отечественные и зарубежные литературные источники за последние 10 лет. Приведены особенности биологии Ustilago tritici и его взаимодействия с растением-хозяином. Рассмотрены возможности и опыт использования различных ПЦР-маркеров как при диагностике и изучении возбудителя пыльной головни пшеницы, так и в маркер-вспомогательной селекции (MAS-селекции) устойчивых к болезни сортов. Показана значимость ПЦР как одного из наиболее распространенных современных, высокочувствительных, специфичных, быстрых и экономически доступных лабораторных методов детекции возбудителя заболевания, а также изучения его расового состава. Проанализирован перечень известных в настоящее время генов, сортов-доноров и ДНК-маркеров, сцепленных с генами и локусами устойчивости пшеницы к пыльной головне. Приведенные результаты исследований свидетельствуют о наличии достаточно большой базы данных для использования ПЦР-маркеров при создании устойчивых сортов пшеницы.

Wheat (Triticum aestivum L.) is an important and popular crop all over the world. An economically significant decrease in its yield is due to disease infection the most harmful of which is the loose smut (Ustilago tritici (Pers.) Rostr.). The most effective, cost – effective and environmentally friendly way to fight the disease is to create resistant varieties using molecular biological methods. The research gives an analysis of domestic and foreign literary sources over the past 10 years. The features of the biology of Ustilago tritici and its interaction with the host plant are presented. The possibilities and experience of using various PCR markers are considered both in the diagnosis and study of the causative agent of wheat smut, and in marker-assisted breeding (MAS-breeding) of disease-resistant cultivars. The importance of PCR as one of the most widespread modern, highly sensitive, specific, fast and economically affordable laboratory methods for detecting the causative agent of the disease, as well as studying its racial composition, is shown. The list of currently known genes, donor cultivars and DNA markers linked to genes and loci of wheat resistance to dust smut is analyzed. The above research results indicate that there is a sufficiently large database for the use of PCR markers in the creation of resistant wheat cultivars.

Triticum aestivum L.сортUstilago tritici (Pers.) Rostr.расагены устойчивостиДНК-маркерTriticum aestivum L.cultivarUstilago tritici (Pers.) Rostr.raceresistance genesDNA markerработа выполнена при поддержке Минобрнауки РФ в рамках Государственного задания ФГБНУ «Федеральный аграрный научный центр Северо-Востока имени Н. В. Рудницкого» (тема №FNWE-2022-0001).the research was carried out under the support of the Ministry of Science and Higher of the Russian Federation within the state assignment of the Federal Agricultural Research Center of the North-East named N.V. Rudnitsky (topic No. FNWE-2022-0001).ReferencesГончарова Н. З., Терентьев С. Е., Воробьева Е. С. Состояние и развитие российского рынка зерна и муки в условиях международных экономических санкций. Вестник Адыгейского государственного университета. Серия: Экономика. 2022;4(310):55–64. DOI: https://doi.org/10.53598/2410-3683-2022-4-310-55-64 EDN: XMMMCW.Goncharova N. Z., Terentyev S. E., Vorobyova E. S. The state and development of the russian grain and flour market in the context of international economic sanctions. Vestnik Adygeyskogo gosudarstvennogo uni-versiteta. Seriya: Ekonomika = The Bulletin of the Adyghe State University, Series «Economics». 2022;4(310):55–64. (In Russ.). DOI: https://doi.org/10.53598/2410-3683-2022-4-310-55-64Hanson H. Wheat in the third world. New York: Routledge, 2021. pp. 194. DOI: https://doi.org/10.4324/9780429267505Hanson H. Wheat in the third world. New York: Routledge, 2021. pp. 194. DOI: https://doi.org/10.4324/9780429267505Saini D. K., Chahal A., Pal N., Srivastava P., Gupta P. K. Meta-analysis reveals consensus genomic regions associated with multiple disease resistance in wheat (Triticum aestivum L.). Molecular Breeding. 2022;42(3):11. DOI: https://doi.org/10.1007/s11032-022-01282-zSaini D. K., Chahal A., Pal N., Srivastava P., Gupta P. K. Meta-analysis reveals consensus genomic regions associated with multiple disease resistance in wheat (Triticum aestivum L.). Molecular Breeding. 2022;42(3):11. DOI: https://doi.org/10.1007/s11032-022-01282-zJabran M., Ali M. A., Zahoor A., Muhae-Ud-Din G., Liu T., Chen W., Gao L. Intelligent reprogramming of wheat for enhancement of fungal and nematode disease resistance using advanced molecular techniques. Frontiers in Plant Science. 2023;14:1132699. DOI: https://doi.org/10.3389/fpls.2023.1132699Jabran M., Ali M. A., Zahoor A., Muhae-Ud-Din G., Liu T., Chen W., Gao L. Intelligent reprogramming of wheat for enhancement of fungal and nematode disease resistance using advanced molecular techniques. Frontiers in Plant Science. 2023;14:1132699. DOI: https://doi.org/10.3389/fpls.2023.1132699Yan H., Zhang J., Ma D., Yin J. qPCR and loop mediated isothermal amplification for rapid detection of Ustilago tritici. PeerJ. 2019;(7):e7766. DOI: https://doi.org/10.7717/peerj.7766Yan H., Zhang J., Ma D., Yin J. qPCR and loop mediated isothermal amplification for rapid detection of Ustilago tritici. PeerJ. 2019;(7):e7766. DOI: https://doi.org/10.7717/peerj.7766Репникова Е. Г., Зеленева Ю. В., Судникова В. П. Головневые болезни пшеницы на территории центрально-чернозёмного заповедника, выявление источников и доноров устойчивости. Научные труды Северо-Кавказского федерального научного центра садоводства, виноградарства, виноделия. 2020;29:214–221. DOI: https://doi.org/10.30679/2587-9847-2020-29-214-221 EDN: XNREHNRepnikova E. G., Zeleneva Yu. V., Sudnikova V. P. Wheat smut diseases on the central chernozem reserve territory, identification of sources and donors of resistance. Nauchnye trudy Severo-Kavkazskogo federal'nogo nauchnogo tsentra sadovodstva, vinogradarstva, vinodeliya. 2020;29:214–221. (In Russ.). DOI: https://doi.org/10.30679/2587-9847-2020-29-214-221Maulenbay A., Rsaliyev A. Fungal disease tolerance with a focus on wheat: a review. Journal of Fungi. 2024;10(7):482. DOI: https://doi.org/10.3390/jof10070482Maulenbay A., Rsaliyev A. Fungal disease tolerance with a focus on wheat: a review. Journal of Fungi. 2024;10(7):482. DOI: https://doi.org/10.3390/jof10070482Орлова Е. А., Бехтольд Н. П. Характеристика генофонда яровой мягкой пшеницы (Triticum aestivum L.) по устойчивости к пыльной головне в условиях лесостепи Западной Сибири. Вавиловский журнал генетики и селекции. 2019;23(5):551–558. DOI: https://doi.org/10.18699/VJ19.524 EDN: PIVINY.Orlova E. A., Baechtold N. P. characteristics of the gene pool of spring wheat (Triticum aestivum L.) for resistance to loose smut in the forest-steppe of Western Siberia. Vavilovskiy zhurnal genetiki i selektsii. = Vavilov Journal of Genetics and Breeding 2019;23(5):551–558. (In Russ.). DOI: https://doi.org/10.18699/VJ19.524Ганнибал Ф. Б., Гагкаева Т. Ю., Гомжина М. М., Полуэктова Е. В., Гультяева Е. И. Ассоциированные с пшеницей микромицеты и их значимость как возбудителей болезней в России. Вестник защиты растений. 2022;105(4):164–180. DOI: https://doi.org/10.31993/2308-6459-2022-105-4-15508 EDN: KLHPMBGannibal F. B., Gagkaeva T. Yu., Gomzhina M. M., Poluektova E. V., Gultyaeva E. I. Micromycetes associated with wheat and their significance as pathogens in Russia. Vestnik zashchity rasteniy = Plant Protection News. 2022;105(4):164–180. (In Russ.). DOI: https://doi.org/10.31993/2308-6459-2022-105-4-15508Кекало А. Ю., Немченко В. В., Заргарян Н. Ю., Цыпышева М. Ю. Защита зерновых культур от болезней. Куртамыш: Куртамышская типография, 2017. 172 с. Режим доступа: https://www.elibrary.ru/item.asp?id=29053721 EDN: YLUIUBKekalo A. Yu., Nemchenko V. V., Zargaryan N. Yu., Tsypysheva M. Yu. Protection of grain crops from diseases. Kurtamysh: Kurtamyshskaya tipografiya, 2017. 172 p. URL: https://www.elibrary.ru/item.asp?id=29053721Грязнов А. А. Расоспецифическая устойчивость пшеницы к пыльной головне. АПК России. 2018;25(1):25–30. Режим доступа: https://www.elibrary.ru/item.asp?id=32484898 EDN: YPUHGJ.Gryaznov A. A. Racespecific resistance of wheat to loose smut. APK Rossii = Agro-Industrial Complex of Russia. 2018;25(1):25–30. (In Russ.). URL: https://www.elibrary.ru/item.asp?id=32484898Abrahim A. Loose smut of wheat (Ustilago tritici) and its managements. Journal of Biology, Agriculture and Healthcare. 2019;9(8):25–33. DOI: https://doi.org/10.7176/JBAHAbrahim A. Loose smut of wheat (Ustilago tritici) and its managements. Journal of Biology, Agriculture and Healthcare. 2019;9(8):25–33. DOI: https://doi.org/10.7176/JBAHToth J., Pandurangan S., Burt A., Mitchell Fetch J., Kumar S. Marker-assisted breeding of hexaploid spring wheat in the Canadian prairies. Canadian journal of plant science. 2018;99(2):111–127. DOI: http://doi.org/10.1139/cjps-2018-0183Toth J., Pandurangan S., Burt A., Mitchell Fetch J., Kumar S. Marker-assisted breeding of hexaploid spring wheat in the Canadian prairies. Canadian journal of plant science. 2018;99(2):111–127. DOI: http://doi.org/10.1139/cjps-2018-0183Назаров П. А., Балеев Д. Н., Иванова М. И., Соколова Л. М., Каракозова М. В. Инфекционные болезни растений: этиология, современное состояние, проблемы и перспективы защиты растений. Acta Naturae. 2020;12(3):46–59. DOI: https://doi.org/10.32607/actanaturae.11026 EDN: AKBYXI.Nazarov P. A., Baleev D. N., Ivanova M. I., Sokolova L. M., Karakozova M. V. Infectious plant diseases: etiology, current status, problems and prospects in plant protection. Acta Naturae. 2020;12(3):46–59. (In Russ.). DOI: https://doi.org/10.32607/actanaturae.11026Kashyap P. L., Kumar S., Tripathi R., Kumar R. S., Jasrotia P., Singh D. P., Singh G. P. Phylogeography and population structure analysis reveal diversity by gene flow and mutation in Ustilago segetum (Pers.) Roussel tritici causing loose smut of wheat. Frontiers in Microbiology. 2019;10:01072. DOI: https://doi.org/10.3389/fmicb.2019.01072Kashyap P. L., Kumar S., Tripathi R., Kumar R. S., Jasrotia P., Singh D. P., Singh G. P. Phylogeography and population structure analysis reveal diversity by gene flow and mutation in Ustilago segetum (Pers.) Roussel tritici causing loose smut of wheat. Frontiers in Microbiology. 2019;10:01072. DOI: https://doi.org/10.3389/fmicb.2019.01072Kumar S., Knox R. E., Singh A. K., DePauw R. M., Campbell H. L., Isidro-Sanchez J., et al. High-density genetic mapping of a major QTL for resistance to multiple races of loose smut in a tetraploid wheat cross. PLoS One. 2018;13(2):e0192261. DOI: https://doi.org/10.1371/journal.pone.0192261Kumar S., Knox R. E., Singh A. K., DePauw R. M., Campbell H. L., Isidro-Sanchez J., et al. High-density genetic mapping of a major QTL for resistance to multiple races of loose smut in a tetraploid wheat cross. PLoS One. 2018;13(2):e0192261. DOI: https://doi.org/10.1371/journal.pone.0192261Афанасенко О. С. Генетическая защита зерновых культур: итоги и перспективы. Защита и карантин растений. 2020;(9):3–7. Режим доступа: https://elibrary.ru/item.asp?id=43909497 EDN: TYQUEV.Afanasenko O. S. Genetic protection of grain crops: results and prospects. Zashchita i karantin rasteniy. 2020;(9):3–7. (In Russ.). URL: https://elibrary.ru/item.asp?id=43909497Hasan N., Choudhary S., Naaz N., Sharma N., Laskar R. A. Recent advancements in molecular markerassisted selection and applications in plant breeding programmes. Journal of Genetic Engineering and Biotechnology. 2021;19(1):128. DOI: https://doi.org/10.1186/s43141-021-00231-1Hasan N., Choudhary S., Naaz N., Sharma N., Laskar R. A. Recent advancements in molecular markerassisted selection and applications in plant breeding programmes. Journal of Genetic Engineering and Biotechnology. 2021;19(1):128. DOI: https://doi.org/10.1186/s43141-021-00231-1Luo K., He D., Guo J., Li G., Li B., Chen X. Molecular advances in breeding for durable resistance against pests and diseases in wheat: Opportunities and challenges. Agronomy. 2023;13(3):628. DOI: https://doi.org/10.3390/agronomy13030628Luo K., He D., Guo J., Li G., Li B., Chen X. Molecular advances in breeding for durable resistance against pests and diseases in wheat: Opportunities and challenges. Agronomy. 2023;13(3):628. DOI: https://doi.org/10.3390/agronomy13030628Zuo W., Ökmen B., Depotter J. R. L., Ebert M. K., Redkar A., Villamil J. M., Doehlemann G. Molecular interactions between smut fungi and their host plants. Annual Review of Phytopathology. 2019;57:411–430. DOI: https://doi.org/10.1146/annurev-phyto-082718-100139Zuo W., Ökmen B., Depotter J. R. L., Ebert M. K., Redkar A., Villamil J. M., Doehlemann G. Molecular interactions between smut fungi and their host plants. Annual Review of Phytopathology. 2019;57:411–430. DOI: https://doi.org/10.1146/annurev-phyto-082718-100139Nagarajan N., Khan M., Djamei A. Manipulation of auxin signaling by smut fungi during plant colonization. Journal of Fungi. 2023;9(12):1184. DOI: https://doi.org/10.3390/jof9121184Nagarajan N., Khan M., Djamei A. Manipulation of auxin signaling by smut fungi during plant colonization. Journal of Fungi. 2023;9(12):1184. DOI: https://doi.org/10.3390/jof9121184Дружин А. Е. Влияние изменений климата на структуру популяций патогенов яровой пшеницы в Поволжье. Аграрный вестник Юго-Востока. 2010;(1):31–35. Режим доступа: https://www.elibrary.ru/item.asp?id=26725203 EDN: WMVNGF.Druzhin A. E. Effect of climate change on the structure of populations of spring wheat pathogens in the Volga region. Agrarnyy vestnik Yugo-Vostoka = Agrarian Reporterof South-East. 2010;(1):31–35. (In Russ.). URL: https://www.elibrary.ru/item.asp?id=26725203Draz I. S., Darwish A. K., Abou-Elsoud M. S., Elassal A. A., Komeil D. A. Molecular discovery of new allele associated with loose smut resistance gene Ut-X in spring wheat. Agronomy Research. 2021;19(1):74–82. DOI: https://doi.org/10.15159/AR.21.055Draz I. S., Darwish A. K., Abou-Elsoud M. S., Elassal A. A., Komeil D. A. Molecular discovery of new allele associated with loose smut resistance gene Ut-X in spring wheat. Agronomy Research. 2021;19(1):74–82. DOI: https://doi.org/10.15159/AR.21.055Сюков В. В., Поротькин С. Е. Генетика устойчивости мягкой пшеницы (Triticum aestivum L.) к пыльной головне (Ustilago tritici (Pers.) Jens.) (обзор). Вавиловский журнал генетики и селекции. 2015;18(3):517–522. Режим доступа: https://elibrary.ru/item.asp?id=22479659 EDN: SXXZIR.Syukov V. V., Porotkin S. E. Genetics of common wheat (Triticum aestivum L.) resistance to loose smut (Ustilago tritici (Pers.) jens.) (review). Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2015;18(3):517–522. (In Russ.). URL: https://elibrary.ru/item.asp?id=22479659Shafikova T. N., Omelichkina Yu. V. Evolution of views on plant immunity: from Flor’s “gene-for-gene” theory to the “zig-zag model” developed by Jones and Dangl. Izvestiya vuzov. Prikladnaya khimiya i biotekhnologiya = Proceedings of Universities. Applied Chemistry and Biotechnology. 2020;10(3):424–438. (In Russ.). DOI: https://doi.org/10.21285/2227-2925-2020-10-3-424-438Shafikova T. N., Omelichkina Yu. V. Evolution of views on plant immunity: from Flor’s “gene-for-gene” theory to the “zig-zag model” developed by Jones and Dangl. Izvestiya vuzov. Prikladnaya khimiya i biotekhnologiya = Proceedings of Universities. Applied Chemistry and Biotechnology. 2020;10(3):424–438. (In Russ.). DOI: https://doi.org/10.21285/2227-2925-2020-10-3-424-438Ökmen B., Schwammbach D., Bakkeren G., Neumann U., Doehlemann G. The Ustilago hordei-barley interaction is a versatile system for characterization of fungal effectors. Journal of Fungi. 2021;7(2):86. DOI: https://doi.org/10.3390/jof7020086Ökmen B., Schwammbach D., Bakkeren G., Neumann U., Doehlemann G. The Ustilago hordei-barley interaction is a versatile system for characterization of fungal effectors. Journal of Fungi. 2021;7(2):86. DOI: https://doi.org/10.3390/jof7020086Wunderle J., Leclerque A., Schaffrath U., Slusarenko A., Koch E. Assessment of the loose smut fungi (Ustilago nuda and U. tritici) in tissues of barley and wheat by fluorescence microscopy and real-time PCR. European journal of plant pathology. 2012;133:865–875. DOI: https://doi.org/10.1007/s10658-012-0010-9Wunderle J., Leclerque A., Schaffrath U., Slusarenko A., Koch E. Assessment of the loose smut fungi (Ustilago nuda and U. tritici) in tissues of barley and wheat by fluorescence microscopy and real-time PCR. European journal of plant pathology. 2012;133:865–875. DOI: https://doi.org/10.1007/s10658-012-0010-9Francesconi S. High-throughput and point-of-care detection of wheat fungal diseases: Potentialities of molecular and phenomics techniques toward in-field applicability. Frontiers in Agronomy. 2022;4:980083. DOI: https://doi.org/10.3389/fagro.2022.980083Francesconi S. High-throughput and point-of-care detection of wheat fungal diseases: Potentialities of molecular and phenomics techniques toward in-field applicability. Frontiers in Agronomy. 2022;4:980083. DOI: https://doi.org/10.3389/fagro.2022.980083Башкирова И. Г., Каримова Е. В., Смирнова И. П. Исследование праймеров для диагностики фитоплазм из группы Apple proliferation. Фитосанитария. Карантин растений. 2022;(3):26–36. Режим доступа: https://elibrary.ru/item.asp?id=51314769 EDN: FZTABW.Bashkirova I. G., Karimova E. V., Smirnova I. P. Study of primers for the diagnosis of phytoplasmas from the apple proliferation group. Fitosanitariya. Karantin rasteniy = Plant Health and Quarantine. 2022;(3):26–36. (In Russ.). URL: https://elibrary.ru/item.asp?id=51314769Камченков А. М., Цветкова Ю. В., Кузнецова А. А., Дудченко И. П., Усманова Г. Р. Оценка применимости классических и молекулярных методов диагностики возбудителя Bipolaris zeicola (Stout) Shoemaker в лабораторных условиях. Фитосанитария. Карантин растений. 2022;(4):33–45. DOI: https://doi.org/10.69536/g6406-7929-8405-a EDN: RHLXLE.Kamchenkov A. V., Tsvetkova Yu. V., Kuznetsova A. A., Duchenko I. P., Usmanova G. R. Evaluation of the applicability of classical and molecular methods for diagnosing the phytopathogen Bipolaris zeicola (Stout) Shoemaker in laboratory conditions. Fitosanitariya. Karantin rasteniy = Plant Health and Quarantine. 2022;(4):33-45. (In Russ.). DOI: https://doi.org/10.69536/g6406-7929-8405-aБессолицына Е. А., Тулинов А. Г., Новоселова Н. В., Харина А. В. Разработка ПЦР-тест системы для выявления вируса картофеля Y. Известия Коми научного центра УрО РАН. 2023;7(65):5–11. DOI: https://doi.org/10.19110/1994-5655-2023-7-5-11 EDN: PYTGKE.Bessolitsyna E. A., Tulinov A. G., Novoselova N. V., Kharina A. V. Development of a PCR test system for the detection of potato virus Y. Izvestiya Komi nauchnogo tsentra UrO RAN = Proceedings of the Komi science centre Ural branch Russian academy of sciences. 2023;7(65):5–11. (In Russ.). DOI: https://doi.org/10.19110/1994-5655-2023-7-5-11Willits D. A., Sherwood J. E. Polymerase chain reaction detection of Ustilago hordei in leaves of susceptible and resistant barley varieties. Phytopathology. 1999;89(3):212–217. DOI: https://doi.org/10.1094/PHYTO.1999.89.3.212Willits D. A., Sherwood J. E. Polymerase chain reaction detection of Ustilago hordei in leaves of susceptible and resistant barley varieties. Phytopathology. 1999;89(3):212–217. DOI: https://doi.org/10.1094/PHYTO.1999.89.3.212Omara R. I., Sehsah M. D., Shaheen D. M., Saad El-Din H. I., Abdelghany R., Mandour A. M., Shahin A. A. A quick PCR detection of Ustilago tritici for early control of loose smut in wheat using TiO2 and ZnO nanoparticles. Egyptian Journal of Agricultural Research. 2023;101(4):1112–1123. DOI: https://doi.org/10.21608/EJAR.2023.242715.1448Omara R. I., Sehsah M. D., Shaheen D. M., Saad El-Din H. I., Abdelghany R., Mandour A. M., Shahin A. A. A quick PCR detection of Ustilago tritici for early control of loose smut in wheat using TiO2 and ZnO nanoparticles. Egyptian Journal of Agricultural Research. 2023;101(4):1112–1123. DOI: https://doi.org/10.21608/EJAR.2023.242715.1448Randhawa H. S., Popovic Z., Menzies J., Knox R., Fox S. Genetics and identification of molecular markers linked to resistance to loose smut (Ustilago tritici) race T33 in durum wheat. Euphytica. 2009;169:151–157. DOI https://doi.org/10.1007/s10681-009-9903-xRandhawa H. S., Popovic Z., Menzies J., Knox R., Fox S. Genetics and identification of molecular markers linked to resistance to loose smut (Ustilago tritici) race T33 in durum wheat. Euphytica. 2009;169:151–157. DOI https://doi.org/10.1007/s10681-009-9903-xKassa M. T., Menzies J. G., McCartney C. A. Mapping of a resistance gene to loose smut (Ustilago tritici) from the Canadian wheat breeding line BW278. Molecular Breeding. 2015;35(9):180. DOI: https://doi.org/10.1007/s11032-015-0369-3Kassa M. T., Menzies J. G., McCartney C. A. Mapping of a resistance gene to loose smut (Ustilago tritici) from the Canadian wheat breeding line BW278. Molecular Breeding. 2015;35(9):180. DOI: https://doi.org/10.1007/s11032-015-0369-3Mishra K. K., Kant L., Kumari J., Kumar A. Mining of the national gene bank collection identifies resistance sources for loose smut of wheat in Northern Himalayan conditions. Indian Phytopathology. 2022;75(4):1179–1183. DOI: https://doi.org/10.1007/s42360-022-00540-6Mishra K. K., Kant L., Kumari J., Kumar A. Mining of the national gene bank collection identifies resistance sources for loose smut of wheat in Northern Himalayan conditions. Indian Phytopathology. 2022;75(4):1179–1183. DOI: https://doi.org/10.1007/s42360-022-00540-6Дружин А. Е., Крупнов В. А. Пшеница и пыльная головня. Саратов: Саратовский университет, 2008. 164 с. Режим доступа: https://elibrary.ru/item.asp?id=19512762 EDN: QKZYIL.Druzhin A. E., Krupnov V. A. Wheat and loose smut. Saratov: Saratovskiy universitet, 2008. 164 p. URL: https://elibrary.ru/item.asp?id=19512762Дружин А. Е. Расовая дифференциация Ustilаgо tritiсi (Реrs). Rоstr. в Саратовской области с использованием канадских и советских сортов-дифференциаторов. Аграрный вестник Юго-Востока. 2009;(2):18–22. Режим доступа: https://elibrary.ru/item.asp?id=26725161 EDN: WMVMQB.Druzhin A. E. Races differentiation Ustilago tritici (Pers.) Jens. in the Saratov area using canadian and soviet cultivars – differentials. Agrarnyy vestnik Yugo-Vostoka = Agrarian Reporterof South-East. 2009;(2):18–22. (In Russ.). URL: https://elibrary.ru/item.asp?id=26725161Nielsen J. J., Thomas P. Loose smut. Chapter 4. In: R. D. Wilcoxson and E. E. Saari Bunt and smut diseases of wheat. Loose smut. Concepts and methods of diseases management. Mexico, D.F. CIMMYT, 1996. pp. 33–47. URL: https://www.yumpu.com/en/document/view/11350921/bunt-and-smut-diseases-of-wheat-cimmytNielsen J. J., Thomas P. Loose smut. Chapter 4. In: R. D. Wilcoxson and E. E. Saari Bunt and smut diseases of wheat. Loose smut. Concepts and methods of diseases management. Mexico, D.F. CIMMYT, 1996. pp. 33–47. URL: https://www.yumpu.com/en/document/view/11350921/bunt-and-smut-diseases-of-wheat-cimmytКривченко В. И., Мягкова Д. В., Щелко Л. Г., Тимошенко З. В. Изучение устойчивости зерновых культур и расового состава возбудителей головневых болезней. Л., 1978. 107 с.Krivchenko V. I., Myagkova D. V., Shchelko L. G., Timoshenko Z. V. Study of the stability of grain crops and the racial composition of the causative agents of head diseases. Leningrad, 1978. 107 p.Karwasra S. S., Mukherjee A. K., Swain S. C., Mohapatra T., Sharma R. P. Evaluation of RAPD, ISSR and AFLP markers for characterization of the loose smut fungus Ustilago tritici. Journal of Plant Biochemistry and Biotechnology. 2002;11:99–103. URL: https://link.springer.com/article/10.1007/BF03263143Karwasra S. S., Mukherjee A. K., Swain S. C., Mohapatra T., Sharma R. P. Evaluation of RAPD, ISSR and AFLP markers for characterization of the loose smut fungus Ustilago tritici. Journal of Plant Biochemistry and Biotechnology. 2002;11:99–103. URL: https://link.springer.com/article/10.1007/BF03263143Popovic Z., Menzies J. G. Intensive and extensive sampling techniques used to measure genetic diversity of Ustilago tritici, using virulence and DNA polymorphism. Canadian journal of plant pathology. 2006;28(2):197–207. DOI: https://doi.org/10.1080/07060660609507287Popovic Z., Menzies J. G. Intensive and extensive sampling techniques used to measure genetic diversity of Ustilago tritici, using virulence and DNA polymorphism. Canadian journal of plant pathology. 2006;28(2):197–207. DOI: https://doi.org/10.1080/07060660609507287Randhawa H. S., Matheson F., Menzies J. G., Fox S. L. Molecular and virulence relationships among races of Ustilago tritici collected from durum and bread wheat. Canadian Journal of Plant Pathology. 2009;31(2):220–231. DOI: https://doi.org/10.1080/07060660909507595Randhawa H. S., Matheson F., Menzies J. G., Fox S. L. Molecular and virulence relationships among races of Ustilago tritici collected from durum and bread wheat. Canadian Journal of Plant Pathology. 2009;31(2):220–231. DOI: https://doi.org/10.1080/07060660909507595Sharma P., Shefali Pandey B., Muthusamy S. K., Kumar S., Saharan M. S., Kumar S., et al. Development and validation of microsatellite markers for Karnal bunt (Tilletia indica) and loose smut (Ustilago segetum tritici) of wheat from related fungal species. Journal of Phytopathology. 2018;166(10):729–738. DOI: https://doi.org/10.1111/jph.12756Sharma P., Shefali Pandey B., Muthusamy S. K., Kumar S., Saharan M. S., Kumar S., et al. Development and validation of microsatellite markers for Karnal bunt (Tilletia indica) and loose smut (Ustilago segetum tritici) of wheat from related fungal species. Journal of Phytopathology. 2018;166(10):729–738. DOI: https://doi.org/10.1111/jph.12756Nielsen J. J. Inheritance of virulence of Ustilago tritici on the differential cultivars Carma, Red Bobs and a derivative of the cross Thatcher x Regent. Canadian journal of botany. 1982;60:1191–1193. DOI: https://doi.org/10.1139/b82-148Nielsen J. J. Inheritance of virulence of Ustilago tritici on the differential cultivars Carma, Red Bobs and a derivative of the cross Thatcher x Regent. Canadian journal of botany. 1982;60:1191–1193. DOI: https://doi.org/10.1139/b82-148Thambugala D., Menzies J. G., Knox R. E., Campbell H. L., McCarthney C. A. Genetic analysis of loose smut (Ustilago tritici) resistance in Sonop spring wheat. BMC Plant Biology. 2020;20(1):314. DOI: https://doi.org/10.1186/s12870-020-02525-xThambugala D., Menzies J. G., Knox R. E., Campbell H. L., McCarthney C. A. Genetic analysis of loose smut (Ustilago tritici) resistance in Sonop spring wheat. BMC Plant Biology. 2020;20(1):314. DOI: https://doi.org/10.1186/s12870-020-02525-xKnox R. E., Campbell H. L., Clarke F. R., Menzies J. G., Popovic Z., Procunier J. D., et al. Quantitative trait loci for resistance in wheat (Triticum aestivum) to Ustilago tritici. Canadian Journal of Plant Pathology. 2014;36(2):187–201. DOI: http://dx.doi.org/10.1080/07060661.2014.905497Knox R. E., Campbell H. L., Clarke F. R., Menzies J. G., Popovic Z., Procunier J. D., et al. Quantitative trait loci for resistance in wheat (Triticum aestivum) to Ustilago tritici. Canadian Journal of Plant Pathology. 2014;36(2):187–201. DOI: http://dx.doi.org/10.1080/07060661.2014.905497Kassa M. T., Menzies J. G., McCartney C. A. Mapping of the loose smut resistance gene Ut6 in wheat (Triticum aestivum L.). Molecular breeding. 2014;33:569–576. DOI: https://doi.org/10.1007/s11032-013-9973-2Kassa M. T., Menzies J. G., McCartney C. A. Mapping of the loose smut resistance gene Ut6 in wheat (Triticum aestivum L.). Molecular breeding. 2014;33:569–576. DOI: https://doi.org/10.1007/s11032-013-9973-2Procunier J. D., Gray M. A., Howes N. K., Knox R. E., Bernier A. M. DNA markers linked to a T10 loose smut resistance gene in wheat (Triticum aestivum L.). Genome. 1997;40(2):176–179. DOI: https://doi.org/10.1139/g97-025Procunier J. D., Gray M. A., Howes N. K., Knox R. E., Bernier A. M. DNA markers linked to a T10 loose smut resistance gene in wheat (Triticum aestivum L.). Genome. 1997;40(2):176–179. DOI: https://doi.org/10.1139/g97-025Colasuonno P., Marcotuli I., Gadaleta A., Soriano M. From genetic maps to QTL cloning: an overview for durum wheat. Plants. 2021;10(2):315. DOI: https://doi.org/10.3390/plants10020315Colasuonno P., Marcotuli I., Gadaleta A., Soriano M. From genetic maps to QTL cloning: an overview for durum wheat. Plants. 2021;10(2):315. DOI: https://doi.org/10.3390/plants10020315Kaur B., Bhatia D., Mavi G. S. Eighty years of gene-for-gene relationship and its applications in identification and utilization of R genes. Journal of genetics. 2021;100(2):50. DOI: https://doi.org/10.1007/s12041-021-01300-7Kaur B., Bhatia D., Mavi G. S. Eighty years of gene-for-gene relationship and its applications in identification and utilization of R genes. Journal of genetics. 2021;100(2):50. DOI: https://doi.org/10.1007/s12041-021-01300-7Hafeez A., Sanu A., Ghosh S., Gilbert D., Bowden R. L., Wulff B. B. N. Creation and judicious application of a wheat resistance gene atlas. Molecular Plant. 2021;4(7):1053–1070. DOI: https://doi.org/10.1016/j.molp.2021.05.014Hafeez A., Sanu A., Ghosh S., Gilbert D., Bowden R. L., Wulff B. B. N. Creation and judicious application of a wheat resistance gene atlas. Molecular Plant. 2021;4(7):1053–1070. DOI: https://doi.org/10.1016/j.molp.2021.05.014Хлесткина Е. К. Молекулярные методы анализа структурно-функциональной организации генов и геномов высших растений. Вавиловский журнал генетики и селекции. 2011;15(4):757–768. Режим доступа: https://elibrary.ru/item.asp?id=17317750 EDN: OOZBTB.Khlestkina E. K. Molecular methods of the analysis of the structural and functional organization of genes and genomes in higher plants. Vavilovskiy zhurnal genetiki i selektsii = Vavilov Journal of Genetics and Breeding. 2011;15(4):757–768. (In Russ.). URL: https://elibrary.ru/item.asp?id=17317750Saini D. K., Srivastava P., Pal N., Gupta P. K. Meta QTLs, ortho-meta-QTLs and candidate genes for grain yield and associated traits in wheat (Triticum aestivum L.). Theoretical and Applied Genetics. 2022;135(3):1049–1081. DOI https://doi.org/10.1007/s00122-021-04018-3Saini D. K., Srivastava P., Pal N., Gupta P. K. Meta QTLs, ortho-meta-QTLs and candidate genes for grain yield and associated traits in wheat (Triticum aestivum L.). Theoretical and Applied Genetics. 2022;135(3):1049–1081. DOI https://doi.org/10.1007/s00122-021-04018-3Hassan M. I., Mahmoud A. F., Amein K. A. Bulked segregant analysis to identify SSR markers for loose smut resistance in bread wheat. Scientific Journal of Agricultural Sciences. 2021;3(1):119–130. DOI: https://doi.org/10.21608/sjas.2021.62206.1070Hassan M. I., Mahmoud A. F., Amein K. A. Bulked segregant analysis to identify SSR markers for loose smut resistance in bread wheat. Scientific Journal of Agricultural Sciences. 2021;3(1):119–130. DOI: https://doi.org/10.21608/sjas.2021.62206.1070Garg B., Yashveer S., Taunk J., Singh V., Redhu N. S., Tokas J., et al. Characterization of wheat (Triticum aestivum) genotypes for multiple fungal resistance using functional markers. The Indian Journal of Agricultural Sciences. 2023;93(1):30–35. DOI: https://doi.org/10.56093/ijas.v93i1.129567.Garg B., Yashveer S., Taunk J., Singh V., Redhu N. S., Tokas J., et al. Characterization of wheat (Triticum aestivum) genotypes for multiple fungal resistance using functional markers. The Indian Journal of Agricultural Sciences. 2023;93(1):30–35. DOI: https://doi.org/10.56093/ijas.v93i1.129567.

The authors declare that there are no conflicts of interest present.