SUMMARY. Stem rust caused by the fungus Puccinia graminis Pers. is a dangerous disease of wheat which occurs in all regions of its cultivation. New highly virulent races causing severe yield losses have appeared in recent decades. Sr33 introgressed from Aegilops tauschii is one of the genes conferring resistance against most races of stem rust including Ug99. To develop winter common wheat lines with the gene Sr33 and evaluate a possible effect of the gene on yield traits, we made a cross between the spring line DH31 carrying the Sr33 gene and the winter cultivar Myrkhad followed by marker-assisted selection of winter genotypes with Sr33 beginning from F3. To identify the Sr33 gene, we used PCR with the gene-specific marker Sr33A. Alleles at the storage protein loci of the parental forms were identified using acid polyacrylamide gel electrophoresis and SDS-electrophoresis, as well as the molecular marker MAR for Glu-B1al. As a result of marker-assisted selection, winter F5 lines with the Sr33 gene were developed from the cross DH31 × Myrkhad. The yield traits of F5 spikes of families derived from single F3 spikes with and without Sr33 were analyzed considering that the line DH31 has a specific allele at Gli-D1 from Ae. tauschii, dark glimes, and high molecular weight glutenin subunit alleles associated with high dough strength, in particular Glu-B1al. Comparison of means of yield traits of spikes from families with Sr33 and without it did not reveal significant differences between these two groups. Thus, winter F5 lines with the Sr33 gene from the cross DH31 × Myrkhad may be used in the breeding practice to develop cultivars with high bread-making qualities of flour and stem rust resistance.
Keywords: wheat, Puccinia graminis, race Ug99, stem rust resistance, gene Sr33, marker-assisted selection, breeding lines, winter common wheat
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References
Aktar-Uz-Zaman, M., Tuhina-Khatun, M., Musa Hanafi, et al., Genetic analysis of rust resistance genes in global wheat cultivars: An overview, Biotechnol. Biotechnol. Equip., 2017, vol. 31. pp. 431–445.
Ayliffe, M., Periyannan, S.K., Feechan, A., et al., A simple method for comparing fungal biomass in infected plant tissues, Mol. Plant-Microbe Interact., 2013, vol. 26, no. 6, pp. 658–667. https://doi.org/10.1094/MPMI-12-12-0291-R
Brown, J.K., Yield penalties of disease resistance in crops, Curr. Opin. Plant Biol., 2002, vol. 5, no. 4, pp. 339–344. https://doi.org/10.1016/s1369-5266(02)00270-4
Butow, B.J., Gale, K.R., Ikea, J., et al., Dissemination of the highly expressed Bx7 glutenin subunit (Glu-B1al allele) in wheat as revealed by novel PCR markers and RP-HPLC, Theor. Appl. Genet., 2004, vol. 109, no. 7, pp. 1525–1535. https://doi.org/10.1007/s00122-004-1776-8
Casey, L.W., Lavrencic, P., Bentham, A.R., et al., The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 45, pp. 12856–12861.
Cesaris, S., Moorea, J., Chen, C., et al., Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 36, pp. 10204–10209. https://doi.org/10.1073/pnas.1605483113
Ivashchuk, B.V., Pirko, Ya.V., Spivak, S.I., et al., Analysis of Ukrainian and foreign wheat samples for the presence of stem rust resistance genes using molecular markers, in Faktory eksperimental’noi evolutsii organizmiv (Factors of Experimental Evolution of Organisms), 2018, vol. 22, pp. 132–137. https://doi.org/10.7124/FEEO.v22.937
Jin, Y., Singh, R.P., Ward, R.W., et al., Characterization of seedling infection types and adult plant infection responses of monogenic Sr gene lines to race TTKS of Puccinia graminis f. sp. tritici, Plant Dis., 2007, vol. 91, pp. 1096–1099. https://doi.org/10.1094/PDIS-91-9-1096
Jones, S.S., Dvorak, J., and Qualset, C.O., Linkage relations of Gli-D1, Rg2, and Lr21 on the short arm of chromosome 1D in wheat, Genome, 1990, vol. 33, pp. 937–940. https://doi.org/10.1139/g90-140
Jones, S.S., Dvorak, J., Knott, D.R., and Qualset, C.Q., Use of double-ditelosomic and normal chromosome 1D recombinant substitution lines to map Sr33 on chromosome arm 1DS in wheat, Genome, 1991, vol. 34, pp. 505–508. https://doi.org/10.1139/g91-077
Karelov, A., Kozub, N., Sozinova, O., et al., Wheat genes associated with different types of resistance against stem rust (Puccinia graminis Pers.), Pathogens, 2022, vol. 11, no. 10, p. 1157. https://doi.org/10.3390/pathogens11101157
Kerber, E.R. and Dyck, P.L., Resistance to stem rust and leaf rust of wheat in Aegilops squarrosa and transfer of a gene for stem rust resistance to hexaploid wheat, Proceedings of the Fifth International Wheat Genetics Symposium, 1979, pp. 358–364.
Kozub, N.A., Sozinov, I.A., Sobko, T.A., et al., Variation at storage protein loci in winter common wheat cultivars of the Central Forest-Steppe of Ukraine, Cytol. Genet., 2009, vol. 43, no. 1, pp. 55–62. https://doi.org/10.3103/S0095452709010101
Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 1970, vol. 227, no. 5259, pp. 680–685.
Leonard, K.J. and Szabo, L.J., Stem rust of small grains and grasses caused by Puccinia graminis, Mol. Plant Pathol., 2005, vol. 6, no. 2, pp. 99–111. https://doi.org/10.1111/j.1364-3703.2005.00273.x
Loughman, R. and Jayasena, K.W., Yield loss and fungicide control of stem rust of wheat, Aust. J. Agric. Res., 2005, vol. 56, pp. 91–96. https://doi.org/10.1071/AR04126
McDonald, B.A. and Linde, C., Pathogen population genetics, evolutionary potential, and durable resistance, Annu. Rev. Phytopathol., 2002, vol. 40, pp. 349–379. https://doi.org/10.1146/annurev.phyto.40.120501.101443
McIntosh, R.A., Wellings, C.R., and Park, R.F., Wheat Rusts: An Atlas of Resistance Genes, Canberra: CSIRO, 1995.
Book
Metakovsky, E., Melnik, V., Rodriguez-Quijano, M., et al., A catalog of gliadin alleles: Polymorphism of 20th-century common wheat germplasm, Crop J., 2018, vol. 6, no. 6, pp. 628–641. https://doi.org/10.1016/j.cj.2018.02.003
Nazari, K., Al-Maaroof, E., Kurtulus, E., et al., First report of Ug99 race TTKTT of wheat stem rust (Puccinia graminis f. sp. tritici) in Iraq, Plant Dis., 2021, vol. 105, p. 2719. https://doi.org/10.1094/PDIS-02-21-0404-PDN
Olivera, P., Newcomb, M., Szabo, L.J., et al., Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in Southern Ethiopia in 2013-14, Phytopathology, 2015, vol. 105, no. 7, pp. 917–928. https://doi.org/10.1094/PHYTO-11-14-0302-FI
Olivera Firpo, P.D., Newcomb, M., Flath, K., et al., Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013, Plant Pathol., 2017, vol. 66, pp. 1258–1266. https://doi.org/10.1111/ppa.12674
Olivera, P.D., Sikharulidze, Z., Dumbadze, R., et al., Presence of a sexual population of Puccinia graminis f. sp. tritici in Georgia provides a hotspot for genotypic and phenotypic diversity, Phytopathology, 2019, vol. 109, no. 12, pp. 2152–2160. https://doi.org/10.1094/PHYTO-06-19-0186-R
Olivera, P.D., Szabo, L., Kokhmetova, A., et al., Puccinia graminis f. sp. tritici population causing recent wheat stem rust epidemics in Kazakhstan is highly diverse and includes novel virulences, Phytopathology, 2022a, vol. 112, no. 11, pp. 2403–2415. https://doi.org/10.1094/phyto-08-21-0320-r
Olivera, P.D., Villegas, D., Cantero-Martínez, C., et al., A unique race of the wheat stem rust pathogen with virulence on Sr31 identified in Spain and reaction of wheat and durum cultivars to this race, Plant Pathol., 2022b, vol. 71, pp. 873–889. https://doi.org/10.1111/ppa.13530
Olson, E.L., Brown-Guedira, G., Marshall, D., et al., Development of wheat lines having a small introgressed segment carrying stem rust resistance gene Sr22, Crop Sci., 2010, vol. 50, pp. 1823–1830. https://doi.org/10.2135/cropsci2009.11.0652
Patpour, M., Hovmøller, S.M., and Justesen, A.F., Emergence of virulence to SrTmp in the Ug99 race group of wheat stem rust, Puccinia graminis f. sp. tritici, in Africa, Plant Dis., 2016, vol. 100, no. 2, pp. 522–552. https://doi.org/10.1094/PDIS-06-15-0668-PDN
Patpour, M., Hovmøller, M.S., Rodriguez-Algaba, J., et al., Wheat stem rust back in Europe: Diversity, prevalence and impact on host resistance, Front. Plant Sci., 2022, vol. 13, p. 882440. https://doi.org/10.3389/fpls.2022.882440
Payne, P.I. and Lawrence, G., Catalogue of alleles for the complex gene loci, Glu-A1, Glu-B1, Glu-D1 which code for high-molecular-weight subunits of glutenin in hexaploid wheat, Cereal Res. Commun., 1983, vol. 11, pp. 29–34.
Periyannan, S., Moore, J., Ayliffe, M., et al., The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99, Science, 2013, vol. 341, pp. 786–788. https://doi.org/10.1126/science.1239028
Pretorius, Z.A., Singh, R.P., Wagoire, W.W., et al., Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda, Plant Dis., 2000, vol. 84, no. 2, pp. 203. https://doi.org/10.1094/PDIS.2000.84.2.203B
Sambasivam, P.K., Bansal, U.K., Hayden, M., et al., Identification of markers linked with stem rust resistance genes Sr33 and Sr45, Proceedings of the 11th International Wheat Genetics Symposium, 2008.
Singh, R.P., Hodson, D.P., Huerta-Espino, J., et al., The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production, Annu. Rev. Phytopathol., 2011, vol. 49, pp. 465–481. https://doi.org/10.1146/annurev-phyto-072910-095423
Stokstad, E., Deadly wheat fungus threatens world’s breadbaskets, Science, 2007, vol. 315, pp. 1786–1787. https://doi.org/10.1126/science.315.5820.1786
The, T.T., Latter, B.D.H., McIntosh, R.A., et al., Grain yields of near isogenic lines with added genes for stem rust resistance, in Proceedings of the Seventh International Wheat Genetics Symposium, Miller, T.E. and Koebner, R.M.D., Eds., Cambridge: Institute of Plant Sciences, 1988.
Wrigley, C.W., Asenstorfer, R., Batey, I.L., et al., The biochemical and molecular basis of wheat quality, in Wheat: Science and Trade, Carver, B.F., Ed., Oxford: Wiley-Blackwell, 2009, pp. 495–520.
Wu, X.X., Lin, Q.J., Ni, X.Y., et al., Characterization of wheat monogenic lines with known Sr genes and wheat lines with resistance to the Ug99 race group for resistance to prevalent races of Puccinia graminis f. sp. tritici in China, Plant Dis., 2020, vol. 104, no. 7, pp. 1939–1943. https://doi.org/10.1094/PDIS-12-19-2736-RE
Wu, X.-X., Zang, C.-Q., Zhang, Y.-Z., et al., Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China, J. Integr. Agric., 2023, vol. 22, no. 6, pp. 1740–1749. https://doi.org/10.1016/j.jia.2022.08.125
Zhang, W., Lukaszewski, A.J., Kolmer, J., et al., Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum, Theor. Appl. Genet., 2005, vol. 111, pp. 573–582. https://doi.org/10.1007/s00122-005-2048-y
Zhang, B., Chi, D., Hiebert, C., et al., Pyramiding stem rust resistance genes to race TTKSK (Ug99) in wheat, Can. J. Plant Pathol., 2019, vol. 41, no. 3, pp. 443–449. https://doi.org/10.1080/07060661.2019.1596983