The use of DNA markers in wheat breeding for resistance to loose smut (review)
https://doi.org/10.30766/2072-9081.2025.26.1.7-20
Abstract
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.
Keywords
About the Authors
Anastasia V. KharinaRussian Federation
Anastasia V. Kharina, PhD in Agricultural Science, researcher
166-a Lenin str., Kirov, 610007
Nina V. Novoselova
Russian Federation
Nina V. Novoselova, junior researcher
166-a Lenin str., Kirov, 610007
References
1. 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/10.53598/2410-3683-2022-4-310-55-64
2. Hanson H. Wheat in the third world. New York: Routledge, 2021. pp. 194. DOI: https://doi.org/10.4324/9780429267505
3. Saini 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-z
4. Jabran 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.2023.1132699
5. Yan 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.7766
6. Repnikova 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/10.30679/2587-9847-2020-29-214-221
7. Maulenbay 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/jof10070482
8. 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/VJ19.524
9. Gannibal 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/10.31993/2308-6459-2022-105-4-15508
10. Kekalo 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=29053721
11. 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=32484898
12. Abrahim 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/JBAH
13. Toth 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-2018-0183
14. 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.11026
15. Kashyap 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.2019.01072
16. Kumar 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.0192261
17. 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=43909497
18. Hasan 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/s43141-021-00231-1
19. Luo 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/agronomy13030628
20. Zuo 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-082718-100139
21. Nagarajan 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/jof9121184
22. 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=26725203
23. Draz 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.21.055
24. 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=22479659
25. Shafikova 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/10.21285/2227-2925-2020-10-3-424-438
26. Ökmen 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/jof7020086
27. Wunderle 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/s10658-012-0010-9
28. Francesconi 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.2022.980083
29. 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=51314769
30. 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-a
31. 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/10.19110/1994-5655-2023-7-5-11
32. Willits 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.1999.89.3.212
33. Omara 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.2023.242715.1448
34. Randhawa 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-x
35. Kassa 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/s11032-015-0369-3
36. Mishra 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/s42360-022-00540-6
37. Druzhin A. E., Krupnov V. A. Wheat and loose smut. Saratov: Saratovskiy universitet, 2008. 164 p. URL: https://elibrary.ru/item.asp?id=19512762
38. 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=26725161
39. Nielsen 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-cimmyt
40. 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.
41. 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/BF03263143
42. Popovic 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/10.1080/07060660609507287
43. Randhawa 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/10.1080/07060660909507595
44. Sharma 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.12756
45. Nielsen 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/b82-148
46. Thambugala 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-x
47. Knox 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/10.1080/07060661.2014.905497
48. Kassa 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/s11032-013-9973-2
49. Procunier 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/g97-025
50. Colasuonno 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/plants10020315
51. Kaur 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/s12041-021-01300-7
52. Hafeez 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.2021.05.014
53. 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=17317750
54. Saini 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/s00122-021-04018-3
55. Hassan 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.2021.62206.1070
56. 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.
Review
For citations:
Kharina A.V., Novoselova N.V. The use of DNA markers in wheat breeding for resistance to loose smut (review). Agricultural Science Euro-North-East. 2025;26(1):7-20. (In Russ.) https://doi.org/10.30766/2072-9081.2025.26.1.7-20