Articles
Characterization of Pyrenophora tritici-repentis (tan spot of wheat) races in Kazakhstan
Madina KUMARBAYEVA- Alma KOKHMETOVA
- Nadezhda KOVALENKO
- Makpal ATISHOVA
- Zhenis KEISHILOV
- Klara AITYMBETOVA
Categories
Published 2022-07-19
Keywords
- Tan spot,
- Ptr ToxA,
- Ptr ToxB,
- Race 1,
- Race 5
How to Cite
[1]
M. KUMARBAYEVA, A. KOKHMETOVA, N. KOVALENKO, M. . ATISHOVA, Z. KEISHILOV, and K. AITYMBETOVA, “Characterization of Pyrenophora tritici-repentis (tan spot of wheat) races in Kazakhstan”, Phytopathol. Mediterr., vol. 61, no. 2, pp. 243–257, Jul. 2022.
Funding data
-
Ministry of Education and Science of the Republic of Kazakhstan
Grant numbers Grant № AP09561672 «Identification of sources of wheat resistant to the Kazakhstani population and dominant races Pyrenophora tritici-repentis using phytopathological and molecular methods» (2021).
Abstract
Tan spot, caused by Pyrenophora tritici-repentis, is an economically important foliar disease of wheat in Kazakhstan. Population structure of the pathogen changes every year due to climate change. This study aimed to characterize the race structure of P. tritici-repentis isolates recovered from wheat in south and north Kazakhstan, and identify tan spot resistance in host genotypes based on disease phenotypes and molecular screening. Virulence profiles were determined within 40 isolates of the pathogen from wheat crops during the 2020 growing season. Seven races, (1, 3, 4, 5, 6, 7 and 8) were identified. A collection of 80 wheat accessions, including promising lines and cultivars from Kazakhstan and Russia, were evaluated for their reactions to races 1 and 5 of the pathogen, and to Ptr ToxA and Ptr ToxB, using greenhouse assessments and molecular markers diagnostic for the Tsn1 and Tsc2 genes. From a practical viewpoint, 18 wheat genotypes were insensitive to the two races and the two Ptr toxins. This resistant germplasm can be used in breeding programmes aiming to develop wheat varieties resistant to P. tritici-repentis.
Downloads
Download data is not yet available.
Metrics
Metrics Loading ...
References
REFERENCES
Abeysekara, N.S., Friesen, T.L., Liu, Z., McClean, P.E., Faris, J.D. 2010. Marker development and saturation mapping of the tan spot Ptr ToxB sensitivity locus Tsc2 in hexaploid wheat. Plant Genome 3: 179189. https://doi.org/10.3835/plantgenome2010.07.0017.
Adhikari, T.B., Bai, J., Meinhardt, S.W., Gurung, S., Myrfeld, M., Patel, J., Ali, S., Gudmestad, N.C., Rasmussen, J.B. 2009. Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 22: 1056–1068. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Ali, S., Francl, L.J., De Wolf, E.D. 1999. First report of Pyrenophora tritici-repentis race 5 from North America. Plant Disease 83: 591–591. https://doi.org/10.1094/pdis.1999.83.6.591a
Anderson, J.A., Efertz, R.J., Faris, J.D., Francl, L.J., Meinhardt, S.W., Gill, B.S. 1999. Genetic analysis of sensitivity to Pyrenophora tritici-repentis necrosis-inducing toxin in durum and common wheat. Phytopathology 89, 293–297. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Balance, G.M., Lamari, L., Bernier, C.C. 1989. Purifcation and characterization of a host selective necrosis toxin from Pyrenophora tritici-repentis. Physiological and Molecular Plant Patholog 35: 203–213. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Benslimane, H., Lamari, L., Benbelkacem, A., Sayoud, R., Bouznad, Z. 2011. Distribution of races of Pyrenophora tritici-repentis in Algeria and identication of a new virulence type. Phytopathologia Mediterranea 50: 203–211. https://doi.org/10.14601/Phytopathol_Mediterr-8746
Benslimane H. 2018. Virulence phenotyping and molecular characterization of a new virulence type of Pyrenophora tritici-repentis the causal agent of Tan Spot. Journal of Plant Pathology 34: 139–142. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Chen, X., Line, R., Leung, H. 1998. Genome scanning for resistance gene analogs in rice, barley, and wheat by high resolution electrophoresis. Theoretical and Applied Genetics 97: 345–355. https://doi.org/10.1007/s001220050905
Chu, C.G., Friesen, T.L., Faris, J.D., Xu, S.S. 2008. Evaluation of seedling resistance to tan spot and Stagonospora nodorum blotch in tetraploid wheat. Crop Science 48: 11071116. https://doi.org/10.2135/cropsci2007.09.0516.
Cotuna, O., Paraschivu, M., Paraschivu, A., Sarateanu, V. 2015. The influence of tillage, crop rotation and residue management on tan spot Drechslera tritici repentis. Died. Shoemaker in winter wheat. Research Journal of Agricultural Sciences 47: 13–21.
Duveiller, E., Dubin, H.J., Reeves, J., McNab, A. Helminthosporium Blights of Wheat: Spot Blotch and Tan Spot. El Batan, Mexico: CIMMYT, 1998.
Engle, J.S., Madden, L.V., Lipps, P.E. 2006. Distribution and pathogenic characterization of Pyrenophora tritici-repentis and Stagonospora nodorum in Ohio. Phytopathology 96: 1355–1362. https://doi.org/10.1094/PHYTO-96-1355
FAO, IFAD, UNICEF, WFP, and WHO. The State of Food Security and Nutrition in the World 2019. Safeguarding against economic slowdowns and downturns (Rome: FAO). 2019, Licence: CC BY-NC-SA 3.0 IGO. http://www.fao.org/3/ca5162en/ca5162en.pdf
Faris, J.D., Anderson, J.A., Francl, L.J., Jordahl, J.G. 1996. Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture fltrate from Pyrenophora tritici-repentis. Phytopathology 86: 459–463. https://doi.org/10.1094/Phyto-86-459
Faris, J.D., Liu, Z., Xu, S.S. 2013. Genetics of tan spot resistance in wheat. Theoretical and Applied Genetics 126: 2197–2217. https://doi.org/10.1007/s00122-013-2157-y
Faris, J.D., Zhang, Z., Lu, H., Lu S., Reddy L., Cloutier S., Fellers J.P., Meinhardt, S.W., Rasmussen, J.B., Xu, S.S., Oliver, R.P., Simons, K.J., Friesen, T.L. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proceedings of the National Academy of Sciences of the USA. 107: 13544-13549. https://doi.org/10.1073/pnas.1004090107.
Friesen, T.L., Ali, S., Kianian, S., Francl, L.J., Rasmussen, J.B. 2003. Role of host sensitivity to Ptr ToxA in development of tan spot of wheat. Phytopathology 93: 397–401. https://doi.org/10.1094/PHYTO.2003.93.4.397
Friesen, T.L., Faris, J.D. 2004. Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theoretical and Applied Genetics 109: 464–471. https://doi.org/10.1007/s00122-004-1678-9
Gamba, F.M., Bassi, F.M., Finckh, M.R. 2017. Race structure of Pyrenophora tritici-repentis in Morocco. Phytopathologia Mediterranea 56: 119–126. https://doi.org/10.14601/Phytopathol_Mediterr-18830
Gamba, F.M., Lamari, L., Brülé-Babel, A.L. 1998. Inheritance of race-specifc necrotic and chlorotic reactions induced by Pyrenophora tritici-repentis in hexaploïd wheats. Canadian Journal of Plant Pathology 20: 401–407.
Gamba, F.M., Strelkov, S.E., Lamari, L. 2012. Virulence of Pyrenophora tritici-repentis in the Southern Cone Region of South America. Canadian Journal of Plant Pathology 34: 545–550. https://doi.org/10.1080/07060661.2012.695750
Giraldo, P., Benavente, E., Manzano-Agugliaro, F., Gimenez, E. 2019. Worldwide research trends on wheat and barley: A bibliometric comparative analysis. Agronomy 9: 352. https://doi.org/10.3390/agronomy9070352
Gultyaeva, E.I., Kokhmetova, A.M., Shreyder, E.R., Shaydayuk, E.L., Atishova, M.N., Madenova, A., Malysheva, A., Galymbek, K. 2020. Genetic variability of perspective btreeding material of spring bread wheat for resistance to leaf rust in russia and Kazakhstan. Bulletin of NAS RK 3: 60-68. https://doi.org/10.32014/2020.2518-1467.70
Gurung, S., Mamidi, S., Bonman, J.M., Xiong, M., Brown-Guedira, G., Adhikari, T.B. 2014. Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat. PloS One 9. https://doi.org/10.1371/journal.pone.0108179
Hosford, R.M.J. 1971. A form of Pyrenophora trichostoma pathogenic to wheat and other grasses. Phytopathology 61: 28–32. https://doi.org/10.1094/Phyto-61-28
Hosford, R.M.J. Tan spot-developing knowledge 1902–1981, virulent races and differentials, methodology, rating systems, other leaf diseases, literature. Tan spot of wheat and related diseases workshop. Ed. R.M. Hosford Jr. Fargo, NDSU, 1982, pp. 1–24.
Kamel, S., Cherif, M., Hafez, M., Despins, T., Aboukhaddour, R. 2019. Pyrenophora tritici–repentis in Tunisia: Race Structure and Effector Genes. Frontiers in Plant Science 10: 1562. https://doi.org/10.3389/fpls.2019.01562
Kariyawasam, G.K., Carter, A.H., Rasmussen, J.B., Faris, J.D., Xu, S.S., Mergoum, M., Liu, Z. 2016. Genetic relationships between racenonspecifc and race specifc interactions in the wheatPyrenophora tritici-repentis pathosystem. Theoretical and Applied Genetics 129: 897908. https://doi.org/0.1007/s001220162670x.
Koishybaev, M.K. Diseases of Crops. Almaty: Bastau Publ., 2002. (in Russian)
Kokhmetova, A., Atishova, M. 2020. Identification wheat genotypes resistant to tan spot Pyrenophora tritici-repentis. Bulletin of NAS RK 2(384): 29-35. https://doi.org/10.32014/2020.2518-1467.38
Kokhmetova, A., Atishova, M., Kumarbayeva, M., Leonova, I.N. 20019. Phytopathological screening and molecular marker analysis of wheat germplasm from Kazakhstan and CIMMYT for resistance to tan spot. Vavilov Journal of Genetics and Breeding 23: 879–886. https://doi.org/10.18699/vj19.562
Kokhmetova, A., Kremneva, O., Volkova, G., Atishova, M., Sapakhova, Z. 2017. Evaluation of wheat cultivars growing in Kazakhstan and Russia for resistance to tan spot. Journal of Plant Pathology 99: 161–167. https://doi.org/10.4454/jpp.v99i1.3812.
Kokhmetova, A., Sehgal, D., Ali, S., Atishova, M., Kumarbayeva, M., Leonova, I., Dreisigacker, S. 2021a. Genome-Wide Association Study of Tan Spot Resistance in a Hexaploid Wheat Collection From Kazakhstan. Frontiers in Genetics 11: 581214. https://doi.org/10.3389/fgene.2020.581214
Kokhmetova, A., Kumarbayeva, M., Atishova, M., Nehe, A., Riley, I.T., Morgounov A. 2021b. Identification of high-yielding wheat genotypes resistant to Pyrenophora tritici-repentis (tan spot). Euphytica 217: 97. https://doi.org/10.1007/s10681-021-02822-y
Kokhmetova, A., Madenova, A., Kampitova, G., Urazaliev, R., Yessimbekova, M., Morgounov, A., Purnhauser, L. 2016. Identification of leaf rust resistance genes in wheat cultivars produced in Kazakhstan. Cereal Research Communications 44(2): 240–250. https://doi.org/10.1556/0806.43.2015.056.
Kokhmetova, A., Sharma, R., Rsaliyev S., Galymbek, K., Baymagambetova, K., Ziyaev, Z., Morgounov A. 2018. Evaluation of Central Asian wheat germplasm for stripe rust resistance. Plant Genetic Resources 16(2): 178-184. https://doi.org/10.1017/S1479262117000132.
Kokhmetova, A.M., Ali, S., Sapakhova, Z., Atishova, M.N. 2018. Identification of genotypes-carriers of resistance to tan spot Ptr ToxA and Ptr ToxB of Pyrenophora tritici-repentis in common wheat collection. Vavilov Journal of Genetics and Breeding 22: 978–986. https://doi.org/10.18699/vj18.440
Kokhmetova, A.M., Atishova, M.N., Galymbek, K. 2020. Identification of wheat germplasm resistant to leaf, stripe and stem rust using molecular markers. Bulletin of NAS RK 2(384): 45-52. https://doi.org/10.32014/2020.2518-1467.40
Kokhmetova, A.M., Atishova, M.N., Madenova, A.K., Kumarbayeva, M.T. 2019. Genotyping of wheat germplasm for resistance to toxins of tan spot Pyrenophora tritici-repentis. J. Biotechnol. Proc. of European Biotechnology Congress. Valencia, Spain, April 11-13, 2019. https://doi.org/10.1016/j.jbiotec.2019.05.188
Kokhmetova, A.M., Kovalenko, N.M., Kumarbaeva, M.T. 2020. Pyrenophora tritici-repentispopulation structure in the Republic of Kazakhstan and identification of wheat germplasm resistant to tan spot. Vavilov Journal of Genetics and Breeding 24(7): 722–729. https://doi.org/10.18699/VJ20.666
Kokhmetova, A.M., Kremneva, O.Yu., Keyshilov, Zh.S., Sultanova, N.Zh. 2016b. Race range and virulence of Pyrenophora tritici-repentis isolates in the Republic of Kazakhstan and the North Caucasus region of Russia. Eurasian Journal of Applied Biotechnology 3: 57-66. (in Russian)
Kremneva, O.Y., Mironenko, N.V., Volkova, G.V., Baranova, O.A., Kim, Y.S. 2021. Kovalenko N.M. Resistance of winter wheat varieties to tan spot in the North Caucasus region of Russia. Saudi Journal of Biological Sciences 28(3): 1787-1794. https://doi.org/10.1016/j.sjbs.2020.12.021.
Kremneva, O.Y., Volkova, G.V. 2007. Diagnostics and methods for assessing the wheat resistance to the causative agent of tan spot. Guidelines. Russian Agricultural Academy Printing House, Moscow. 2007. (in Russian)
Lamari, L., Bernier, C.C. 1989. Evaluation of wheat lines and cultivars to tan spot (P. tritici-repentis) based on lesion type. Canadian Journal of Plant Pathology 11: 49–56. https://doi.org/10.1080/07060668909501146
Lamari, L., Bernier, C.C. 1991. Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora triticirepentis. Phytopathology 81: 1092–1095. https://doi.org/10.1094/Phyto-81-1092
Lamari, L., Gilbert, J., Tekauz, A. 1998. Race differentiation in Pyrenophora tritici-repentis and survey of physiologic variation in western Canada. Canadian Journal of Plant Pathology 20(4): 396-400.
Lamari, L., McCallum, B.D., Depauw, R.M. 2005b. Forensic pathology of Canadian bread wheat: the case of tan spot. Phytopathology 95: 144–152. https://doi.org/10.1094/phyto-95-0144
Lamari, L., Sayoud, R., Boulif, M., Bernier, C.C. 1995. Identification of a new race in Pyrenophora tritici-repentis: implications for the current pathotype classification system. Canadian Journal of Plant Pathology 17(4): 312–318. https://doi.org/10.1080/07060669509500668
Lamari, L., Strelkov, S.E., Yahyaoui, A., Amedov, M., Saidov, M., Djunusova, M., Koichibayev, M. 2005a. Virulence of Pyrenophora triticirepentis in the countries of the Silk Road. Canadian Journal of Plant Pathology 27: 383-388. https://doi.org/10.1080/07060661.2012.695750.
Lamari, L., Strelkov, S.E., Yahyaoui, A., Orabi, J., Smith, R.B. 2003. The identifcation of two new races of Pyrenophora tritici-repentis from the host center of diversity confrms a one-to-one relationship in tan spot of wheat. Phytopathology 93: 391–396. https://doi.org/10.1094/PHYTO.2003.93.4.391
Laribi, M., Gamba, F.M., Hassine, M., Singh, P.K., Yahyaoui, A., Sassi, K. 2019. Race structure and distribution of Pyrenophora tritici-repentis in Tunisia. Phytopathologia Mediterranea 58(3): 473-483. https://doi.org/10.13128/ Phyto-10892
Madenova, A., Sapakhova, Z., Bakirov, S., Galymbek K., Yernazarova, G., Kokhmetova, A., Keishilov Zh. 2021. Screening of wheat genotypes for the presence of common bunt resistance genes. Saudi Journal of Biological Sciences 28: 2816-2823. https://doi.org/10.1016/j.sjbs.2021.02.013
Maraite, H., Mercado-Vergnes, D., Renard, M.-E., Zhanarbekova, A., Duveiller, E. 2006. Relevance of pathogen diversity in management of leaf spot and leaf blight diseases on wheat in Central Asia. Agromeridian 2: 105-114.
Mofat, C.S., See, P.T., Oliver, R.P. 2014. Generation of a ToxA knockout strain of the wheat tan spot pathogen Pyrenophora tritici-repentis. Molecular Plant Pathology 15: 918–926. https://doi.org/10.1111/mpp.12154
Orolaza, N.P., Lamari, L., Balance, G.M. 1995. Evidence of a host-specifc chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Phytopathology 85: 1282–1287. https://doi.org/10.1094/Phyto-85-1282
Ouaar, N., Benbelkacem, A., Singh, P.K., Oumata, S., Benslimane, H. 2021. Reaction of Algerian and international germplasm of wheat against races 1 and 5 of Pyrenophora tritici-repentis the causal agent of tan spot. Cereal Research Communications https://doi.org/10.1007/s42976-021-00161-1
Phuke, R.M., He, X., Juliana, P., Bishnoi, S.K., Singh, G.P., Kabir, M.R., Roy, K.K., Joshi, A.K., Singh, R.P., Singh, P.K. 2020. Association Mapping of Seedling Resistance to Tan Spot (Pyrenophora tritici-repentis Race 1) in CIMMYT and South Asian Wheat Germplasm. Frontiers in Plant Science 11: 1309. https://doi.org/10.3389/fpls.2020.01309
Rees, R.G., Platz, G.J. 1992. Tan spot and its control - some Australian experiences, in Advances in tan spot research. Eds. L.J. Francl, J.M. Krupinsky, M.P. McMullen. Fargo, ND, US: NDSU Agric. Exp. Sta.Publ., 1992., pp. 1–15.
Riede, C.R., Anderson, J.A. 1996. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Science 36(4): 905-909.
Saari, E.E., Prescott, L.M. 1975. A scale for appraising the foliar intensity of wheat diseases. Plant. Dis. Rep. 59, 377–380.
Strelkov, S.E., Lamari, L. 2003. Host-parasite interaction in tan spot Pyrenophora tritici-repentis of wheat. Canadian Journal of Plant Pathology 25: 339–349. https://doi.org/10.1080/07060660309507089
Strelkov, S.E., Lamari, L., Balance, G.M. 1999. Characterization of a host specifc protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 12: 728–732. https://doi.org/10.1094/MPMI.1999.12.8.728
Strelkov, S.E., Lamari, L., Sayoud, R., Smith, R.B. 2002. Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Canadian Journal of Plant Pathology 24: 29–35. https://doi.org/10.1080/07060660109506967
Tekauz, A. 1976. Distribution, severity and relative importance of leaf spot disease of wheat in western Canada in 1974. Canadian Plant Disease Survey 56: 36–40.
Toma’s, A., Feng, G.H., Reeck, G.R., Bockus, W.W., Leach, J.E. 1990. Purifcation of a cultivar specifc toxin from, Pyrenophora triticirepentis, causal agent of tan spot of wheat. Molecular Plant-Microbe Interactions 3: 221–224. https://doi.org/10.1094/MPMI-3-221
Wegulo, S.N. 2011. Tan spot of cereals. Plant health instr. https://doi.org/10.1094/PHI-I-2011-0426-01
Zadoks, J.C., Chang, T.T., Konzak, M.M. 1974. A decimal code for the growth stages of wheat. Weed Research 14: 415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zhanarbekova, A.B., Koishibayev M., Maraite, H., Duveiller, E., Mercado, D.M., Sliamova, N.D. 2005. The distribution of tan spot on wheat and race structure of Drechslera tritici-repentis in Kazakhstan and neighboring CIS countries. In: Proc. Int. Sci. Conf. “Modern Problems of Plant Protection and Quarantine”. Almaty, 2005, 371-376.
Zhang, H.F., Francl, LJ., Jordahl, J.G., Meinhardt, S.W. 1997. Structural and physical properties of necrosis inducing toxin from Pyrenophora tritici-repentis. Phytopathology 87: 154–160. https://doi.org/10.1094/phyto.1997.87.2.154
Zhang, Z., Friesen, T.L., Simons, K.J., Xu, S.S., Faris, J.D. 2009. Development, identifcation, and validation of markers for marker assisted selection against the Stagonospora nodorum toxin sensitivity genes Tsn1 and Snn2 in wheat. Molecular Breeding 23: 3549. https://doi.org/10.1007/s1103200892115.
Abeysekara, N.S., Friesen, T.L., Liu, Z., McClean, P.E., Faris, J.D. 2010. Marker development and saturation mapping of the tan spot Ptr ToxB sensitivity locus Tsc2 in hexaploid wheat. Plant Genome 3: 179189. https://doi.org/10.3835/plantgenome2010.07.0017.
Adhikari, T.B., Bai, J., Meinhardt, S.W., Gurung, S., Myrfeld, M., Patel, J., Ali, S., Gudmestad, N.C., Rasmussen, J.B. 2009. Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 22: 1056–1068. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Ali, S., Francl, L.J., De Wolf, E.D. 1999. First report of Pyrenophora tritici-repentis race 5 from North America. Plant Disease 83: 591–591. https://doi.org/10.1094/pdis.1999.83.6.591a
Anderson, J.A., Efertz, R.J., Faris, J.D., Francl, L.J., Meinhardt, S.W., Gill, B.S. 1999. Genetic analysis of sensitivity to Pyrenophora tritici-repentis necrosis-inducing toxin in durum and common wheat. Phytopathology 89, 293–297. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Balance, G.M., Lamari, L., Bernier, C.C. 1989. Purifcation and characterization of a host selective necrosis toxin from Pyrenophora tritici-repentis. Physiological and Molecular Plant Patholog 35: 203–213. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Benslimane, H., Lamari, L., Benbelkacem, A., Sayoud, R., Bouznad, Z. 2011. Distribution of races of Pyrenophora tritici-repentis in Algeria and identication of a new virulence type. Phytopathologia Mediterranea 50: 203–211. https://doi.org/10.14601/Phytopathol_Mediterr-8746
Benslimane H. 2018. Virulence phenotyping and molecular characterization of a new virulence type of Pyrenophora tritici-repentis the causal agent of Tan Spot. Journal of Plant Pathology 34: 139–142. https://doi.org/10.5423/PPJ.OA.07.2016.0157
Chen, X., Line, R., Leung, H. 1998. Genome scanning for resistance gene analogs in rice, barley, and wheat by high resolution electrophoresis. Theoretical and Applied Genetics 97: 345–355. https://doi.org/10.1007/s001220050905
Chu, C.G., Friesen, T.L., Faris, J.D., Xu, S.S. 2008. Evaluation of seedling resistance to tan spot and Stagonospora nodorum blotch in tetraploid wheat. Crop Science 48: 11071116. https://doi.org/10.2135/cropsci2007.09.0516.
Cotuna, O., Paraschivu, M., Paraschivu, A., Sarateanu, V. 2015. The influence of tillage, crop rotation and residue management on tan spot Drechslera tritici repentis. Died. Shoemaker in winter wheat. Research Journal of Agricultural Sciences 47: 13–21.
Duveiller, E., Dubin, H.J., Reeves, J., McNab, A. Helminthosporium Blights of Wheat: Spot Blotch and Tan Spot. El Batan, Mexico: CIMMYT, 1998.
Engle, J.S., Madden, L.V., Lipps, P.E. 2006. Distribution and pathogenic characterization of Pyrenophora tritici-repentis and Stagonospora nodorum in Ohio. Phytopathology 96: 1355–1362. https://doi.org/10.1094/PHYTO-96-1355
FAO, IFAD, UNICEF, WFP, and WHO. The State of Food Security and Nutrition in the World 2019. Safeguarding against economic slowdowns and downturns (Rome: FAO). 2019, Licence: CC BY-NC-SA 3.0 IGO. http://www.fao.org/3/ca5162en/ca5162en.pdf
Faris, J.D., Anderson, J.A., Francl, L.J., Jordahl, J.G. 1996. Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture fltrate from Pyrenophora tritici-repentis. Phytopathology 86: 459–463. https://doi.org/10.1094/Phyto-86-459
Faris, J.D., Liu, Z., Xu, S.S. 2013. Genetics of tan spot resistance in wheat. Theoretical and Applied Genetics 126: 2197–2217. https://doi.org/10.1007/s00122-013-2157-y
Faris, J.D., Zhang, Z., Lu, H., Lu S., Reddy L., Cloutier S., Fellers J.P., Meinhardt, S.W., Rasmussen, J.B., Xu, S.S., Oliver, R.P., Simons, K.J., Friesen, T.L. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proceedings of the National Academy of Sciences of the USA. 107: 13544-13549. https://doi.org/10.1073/pnas.1004090107.
Friesen, T.L., Ali, S., Kianian, S., Francl, L.J., Rasmussen, J.B. 2003. Role of host sensitivity to Ptr ToxA in development of tan spot of wheat. Phytopathology 93: 397–401. https://doi.org/10.1094/PHYTO.2003.93.4.397
Friesen, T.L., Faris, J.D. 2004. Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theoretical and Applied Genetics 109: 464–471. https://doi.org/10.1007/s00122-004-1678-9
Gamba, F.M., Bassi, F.M., Finckh, M.R. 2017. Race structure of Pyrenophora tritici-repentis in Morocco. Phytopathologia Mediterranea 56: 119–126. https://doi.org/10.14601/Phytopathol_Mediterr-18830
Gamba, F.M., Lamari, L., Brülé-Babel, A.L. 1998. Inheritance of race-specifc necrotic and chlorotic reactions induced by Pyrenophora tritici-repentis in hexaploïd wheats. Canadian Journal of Plant Pathology 20: 401–407.
Gamba, F.M., Strelkov, S.E., Lamari, L. 2012. Virulence of Pyrenophora tritici-repentis in the Southern Cone Region of South America. Canadian Journal of Plant Pathology 34: 545–550. https://doi.org/10.1080/07060661.2012.695750
Giraldo, P., Benavente, E., Manzano-Agugliaro, F., Gimenez, E. 2019. Worldwide research trends on wheat and barley: A bibliometric comparative analysis. Agronomy 9: 352. https://doi.org/10.3390/agronomy9070352
Gultyaeva, E.I., Kokhmetova, A.M., Shreyder, E.R., Shaydayuk, E.L., Atishova, M.N., Madenova, A., Malysheva, A., Galymbek, K. 2020. Genetic variability of perspective btreeding material of spring bread wheat for resistance to leaf rust in russia and Kazakhstan. Bulletin of NAS RK 3: 60-68. https://doi.org/10.32014/2020.2518-1467.70
Gurung, S., Mamidi, S., Bonman, J.M., Xiong, M., Brown-Guedira, G., Adhikari, T.B. 2014. Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat. PloS One 9. https://doi.org/10.1371/journal.pone.0108179
Hosford, R.M.J. 1971. A form of Pyrenophora trichostoma pathogenic to wheat and other grasses. Phytopathology 61: 28–32. https://doi.org/10.1094/Phyto-61-28
Hosford, R.M.J. Tan spot-developing knowledge 1902–1981, virulent races and differentials, methodology, rating systems, other leaf diseases, literature. Tan spot of wheat and related diseases workshop. Ed. R.M. Hosford Jr. Fargo, NDSU, 1982, pp. 1–24.
Kamel, S., Cherif, M., Hafez, M., Despins, T., Aboukhaddour, R. 2019. Pyrenophora tritici–repentis in Tunisia: Race Structure and Effector Genes. Frontiers in Plant Science 10: 1562. https://doi.org/10.3389/fpls.2019.01562
Kariyawasam, G.K., Carter, A.H., Rasmussen, J.B., Faris, J.D., Xu, S.S., Mergoum, M., Liu, Z. 2016. Genetic relationships between racenonspecifc and race specifc interactions in the wheatPyrenophora tritici-repentis pathosystem. Theoretical and Applied Genetics 129: 897908. https://doi.org/0.1007/s001220162670x.
Koishybaev, M.K. Diseases of Crops. Almaty: Bastau Publ., 2002. (in Russian)
Kokhmetova, A., Atishova, M. 2020. Identification wheat genotypes resistant to tan spot Pyrenophora tritici-repentis. Bulletin of NAS RK 2(384): 29-35. https://doi.org/10.32014/2020.2518-1467.38
Kokhmetova, A., Atishova, M., Kumarbayeva, M., Leonova, I.N. 20019. Phytopathological screening and molecular marker analysis of wheat germplasm from Kazakhstan and CIMMYT for resistance to tan spot. Vavilov Journal of Genetics and Breeding 23: 879–886. https://doi.org/10.18699/vj19.562
Kokhmetova, A., Kremneva, O., Volkova, G., Atishova, M., Sapakhova, Z. 2017. Evaluation of wheat cultivars growing in Kazakhstan and Russia for resistance to tan spot. Journal of Plant Pathology 99: 161–167. https://doi.org/10.4454/jpp.v99i1.3812.
Kokhmetova, A., Sehgal, D., Ali, S., Atishova, M., Kumarbayeva, M., Leonova, I., Dreisigacker, S. 2021a. Genome-Wide Association Study of Tan Spot Resistance in a Hexaploid Wheat Collection From Kazakhstan. Frontiers in Genetics 11: 581214. https://doi.org/10.3389/fgene.2020.581214
Kokhmetova, A., Kumarbayeva, M., Atishova, M., Nehe, A., Riley, I.T., Morgounov A. 2021b. Identification of high-yielding wheat genotypes resistant to Pyrenophora tritici-repentis (tan spot). Euphytica 217: 97. https://doi.org/10.1007/s10681-021-02822-y
Kokhmetova, A., Madenova, A., Kampitova, G., Urazaliev, R., Yessimbekova, M., Morgounov, A., Purnhauser, L. 2016. Identification of leaf rust resistance genes in wheat cultivars produced in Kazakhstan. Cereal Research Communications 44(2): 240–250. https://doi.org/10.1556/0806.43.2015.056.
Kokhmetova, A., Sharma, R., Rsaliyev S., Galymbek, K., Baymagambetova, K., Ziyaev, Z., Morgounov A. 2018. Evaluation of Central Asian wheat germplasm for stripe rust resistance. Plant Genetic Resources 16(2): 178-184. https://doi.org/10.1017/S1479262117000132.
Kokhmetova, A.M., Ali, S., Sapakhova, Z., Atishova, M.N. 2018. Identification of genotypes-carriers of resistance to tan spot Ptr ToxA and Ptr ToxB of Pyrenophora tritici-repentis in common wheat collection. Vavilov Journal of Genetics and Breeding 22: 978–986. https://doi.org/10.18699/vj18.440
Kokhmetova, A.M., Atishova, M.N., Galymbek, K. 2020. Identification of wheat germplasm resistant to leaf, stripe and stem rust using molecular markers. Bulletin of NAS RK 2(384): 45-52. https://doi.org/10.32014/2020.2518-1467.40
Kokhmetova, A.M., Atishova, M.N., Madenova, A.K., Kumarbayeva, M.T. 2019. Genotyping of wheat germplasm for resistance to toxins of tan spot Pyrenophora tritici-repentis. J. Biotechnol. Proc. of European Biotechnology Congress. Valencia, Spain, April 11-13, 2019. https://doi.org/10.1016/j.jbiotec.2019.05.188
Kokhmetova, A.M., Kovalenko, N.M., Kumarbaeva, M.T. 2020. Pyrenophora tritici-repentispopulation structure in the Republic of Kazakhstan and identification of wheat germplasm resistant to tan spot. Vavilov Journal of Genetics and Breeding 24(7): 722–729. https://doi.org/10.18699/VJ20.666
Kokhmetova, A.M., Kremneva, O.Yu., Keyshilov, Zh.S., Sultanova, N.Zh. 2016b. Race range and virulence of Pyrenophora tritici-repentis isolates in the Republic of Kazakhstan and the North Caucasus region of Russia. Eurasian Journal of Applied Biotechnology 3: 57-66. (in Russian)
Kremneva, O.Y., Mironenko, N.V., Volkova, G.V., Baranova, O.A., Kim, Y.S. 2021. Kovalenko N.M. Resistance of winter wheat varieties to tan spot in the North Caucasus region of Russia. Saudi Journal of Biological Sciences 28(3): 1787-1794. https://doi.org/10.1016/j.sjbs.2020.12.021.
Kremneva, O.Y., Volkova, G.V. 2007. Diagnostics and methods for assessing the wheat resistance to the causative agent of tan spot. Guidelines. Russian Agricultural Academy Printing House, Moscow. 2007. (in Russian)
Lamari, L., Bernier, C.C. 1989. Evaluation of wheat lines and cultivars to tan spot (P. tritici-repentis) based on lesion type. Canadian Journal of Plant Pathology 11: 49–56. https://doi.org/10.1080/07060668909501146
Lamari, L., Bernier, C.C. 1991. Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora triticirepentis. Phytopathology 81: 1092–1095. https://doi.org/10.1094/Phyto-81-1092
Lamari, L., Gilbert, J., Tekauz, A. 1998. Race differentiation in Pyrenophora tritici-repentis and survey of physiologic variation in western Canada. Canadian Journal of Plant Pathology 20(4): 396-400.
Lamari, L., McCallum, B.D., Depauw, R.M. 2005b. Forensic pathology of Canadian bread wheat: the case of tan spot. Phytopathology 95: 144–152. https://doi.org/10.1094/phyto-95-0144
Lamari, L., Sayoud, R., Boulif, M., Bernier, C.C. 1995. Identification of a new race in Pyrenophora tritici-repentis: implications for the current pathotype classification system. Canadian Journal of Plant Pathology 17(4): 312–318. https://doi.org/10.1080/07060669509500668
Lamari, L., Strelkov, S.E., Yahyaoui, A., Amedov, M., Saidov, M., Djunusova, M., Koichibayev, M. 2005a. Virulence of Pyrenophora triticirepentis in the countries of the Silk Road. Canadian Journal of Plant Pathology 27: 383-388. https://doi.org/10.1080/07060661.2012.695750.
Lamari, L., Strelkov, S.E., Yahyaoui, A., Orabi, J., Smith, R.B. 2003. The identifcation of two new races of Pyrenophora tritici-repentis from the host center of diversity confrms a one-to-one relationship in tan spot of wheat. Phytopathology 93: 391–396. https://doi.org/10.1094/PHYTO.2003.93.4.391
Laribi, M., Gamba, F.M., Hassine, M., Singh, P.K., Yahyaoui, A., Sassi, K. 2019. Race structure and distribution of Pyrenophora tritici-repentis in Tunisia. Phytopathologia Mediterranea 58(3): 473-483. https://doi.org/10.13128/ Phyto-10892
Madenova, A., Sapakhova, Z., Bakirov, S., Galymbek K., Yernazarova, G., Kokhmetova, A., Keishilov Zh. 2021. Screening of wheat genotypes for the presence of common bunt resistance genes. Saudi Journal of Biological Sciences 28: 2816-2823. https://doi.org/10.1016/j.sjbs.2021.02.013
Maraite, H., Mercado-Vergnes, D., Renard, M.-E., Zhanarbekova, A., Duveiller, E. 2006. Relevance of pathogen diversity in management of leaf spot and leaf blight diseases on wheat in Central Asia. Agromeridian 2: 105-114.
Mofat, C.S., See, P.T., Oliver, R.P. 2014. Generation of a ToxA knockout strain of the wheat tan spot pathogen Pyrenophora tritici-repentis. Molecular Plant Pathology 15: 918–926. https://doi.org/10.1111/mpp.12154
Orolaza, N.P., Lamari, L., Balance, G.M. 1995. Evidence of a host-specifc chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Phytopathology 85: 1282–1287. https://doi.org/10.1094/Phyto-85-1282
Ouaar, N., Benbelkacem, A., Singh, P.K., Oumata, S., Benslimane, H. 2021. Reaction of Algerian and international germplasm of wheat against races 1 and 5 of Pyrenophora tritici-repentis the causal agent of tan spot. Cereal Research Communications https://doi.org/10.1007/s42976-021-00161-1
Phuke, R.M., He, X., Juliana, P., Bishnoi, S.K., Singh, G.P., Kabir, M.R., Roy, K.K., Joshi, A.K., Singh, R.P., Singh, P.K. 2020. Association Mapping of Seedling Resistance to Tan Spot (Pyrenophora tritici-repentis Race 1) in CIMMYT and South Asian Wheat Germplasm. Frontiers in Plant Science 11: 1309. https://doi.org/10.3389/fpls.2020.01309
Rees, R.G., Platz, G.J. 1992. Tan spot and its control - some Australian experiences, in Advances in tan spot research. Eds. L.J. Francl, J.M. Krupinsky, M.P. McMullen. Fargo, ND, US: NDSU Agric. Exp. Sta.Publ., 1992., pp. 1–15.
Riede, C.R., Anderson, J.A. 1996. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Science 36(4): 905-909.
Saari, E.E., Prescott, L.M. 1975. A scale for appraising the foliar intensity of wheat diseases. Plant. Dis. Rep. 59, 377–380.
Strelkov, S.E., Lamari, L. 2003. Host-parasite interaction in tan spot Pyrenophora tritici-repentis of wheat. Canadian Journal of Plant Pathology 25: 339–349. https://doi.org/10.1080/07060660309507089
Strelkov, S.E., Lamari, L., Balance, G.M. 1999. Characterization of a host specifc protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 12: 728–732. https://doi.org/10.1094/MPMI.1999.12.8.728
Strelkov, S.E., Lamari, L., Sayoud, R., Smith, R.B. 2002. Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Canadian Journal of Plant Pathology 24: 29–35. https://doi.org/10.1080/07060660109506967
Tekauz, A. 1976. Distribution, severity and relative importance of leaf spot disease of wheat in western Canada in 1974. Canadian Plant Disease Survey 56: 36–40.
Toma’s, A., Feng, G.H., Reeck, G.R., Bockus, W.W., Leach, J.E. 1990. Purifcation of a cultivar specifc toxin from, Pyrenophora triticirepentis, causal agent of tan spot of wheat. Molecular Plant-Microbe Interactions 3: 221–224. https://doi.org/10.1094/MPMI-3-221
Wegulo, S.N. 2011. Tan spot of cereals. Plant health instr. https://doi.org/10.1094/PHI-I-2011-0426-01
Zadoks, J.C., Chang, T.T., Konzak, M.M. 1974. A decimal code for the growth stages of wheat. Weed Research 14: 415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zhanarbekova, A.B., Koishibayev M., Maraite, H., Duveiller, E., Mercado, D.M., Sliamova, N.D. 2005. The distribution of tan spot on wheat and race structure of Drechslera tritici-repentis in Kazakhstan and neighboring CIS countries. In: Proc. Int. Sci. Conf. “Modern Problems of Plant Protection and Quarantine”. Almaty, 2005, 371-376.
Zhang, H.F., Francl, LJ., Jordahl, J.G., Meinhardt, S.W. 1997. Structural and physical properties of necrosis inducing toxin from Pyrenophora tritici-repentis. Phytopathology 87: 154–160. https://doi.org/10.1094/phyto.1997.87.2.154
Zhang, Z., Friesen, T.L., Simons, K.J., Xu, S.S., Faris, J.D. 2009. Development, identifcation, and validation of markers for marker assisted selection against the Stagonospora nodorum toxin sensitivity genes Tsn1 and Snn2 in wheat. Molecular Breeding 23: 3549. https://doi.org/10.1007/s1103200892115.