Virulence diversity of the yellow rust pathogen population in Dagestan

Background. Yellow rust incidence on Triticum L. has been observed to surge up in Dagestan in recent years, facilitating selection of highly resistant genotypes. Information on the effectiveness of Yr genes and the pathogen’s virulence and racial composition is needed to interpret field assessment data correctly. The objective of this study was to describe the virulence of the Dagestan population of Puccinia striiformis West. at the seedling stage, evaluate the resistance of differentiators to yellow rust in the field, and identify invasive PstS1 and PstS2 races.

Materials and methods. Leaves with urediniopustules were collected from bread wheat accessions at Dagestan Experiment Station of VIR (DЕS VIR) in 2020–2022. Virulence was analyzed in the laboratory using 14 AvYr lines (Avocet NIL) and 15 differential wheat cultivars. Age-specific resistance of virulence testers under high natural infection pressure was studied in the field of DES VIR. A set of SCAR markers (SCP19M24a1, SCP19M24a2, SCP19M26a1, and SCP19M26a2) were used to identify invasive races.

Results and discussion. Avocet lines with Yr5, Yr10, Yr15, Yr24, and Yr26, and cv. ‘Moro’ (Yr10, YrMor) manifested resistance to all isolates. Virulence to Yr17 was detected only in the isolates from cvs. ‘Graf’ and ‘Svarog’ carrying this gene, and ‘Siete Ceros’. The Dagestan collection demonstrated high genetic diversity. Common phenotypes were identified on cv. ‘Graf’ in 2021 and 2020. There was no temporal differentiation between pathogen collections in the years of testing. High field resistance to yellow rust was recorded in lines with Yr5, Yr8, Yr10, Yr15 and Yr24, and in cvs. ‘Moro’, ‘Compair’, ‘Carstens’ and ‘Spaldings Prolific’. Cvs. ‘Reichersberg 42’ and ‘Heines Peko Vilmorin 23’ were resistant in 2020 and 2022, and moderately affected (up to 10%) in 2021. Molecular analysis identified all three isolates belonging to the invasive PstS2 group on cv. ‘Siete Cerros’ and L 650 in 2021, and cv. ‘Vassa’ in 2022.

1. Bouvet L., Holdgate S., James L., Thomas J., Mackay I.J., Cockram J. The evolving battle between yellow rust and wheat: implications for global food security. Theoretical and Applied Genetics. 2022;135(3):741-753. DOI: 10.1007/s00122-021-03983-z

2. Chen X., Wang M., Wan A., Bai Q., Li M., López P.F. et al. Virulence characterization of Puccinia striiformis f. sp. tritici collections from six countries in 2013 to 2020. Canadian Journal of Plant Pathology. 2021;43 Suppl 2:308-322. DOI: 10.1080/07060661.2021.1958259

3. Chen X.M. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology. 2005;27(3):314-337. DOI: 10.1080/07060660509507230

4. El Amil R., Ali S., Bahri B., Leconte M., de Vallavieille-Pope C., Nazari K. Pathotype diversification in the invasive PstS2 clonal lineage of Puccinia striiformis f. sp. tritici causing yellow rust on durum and bread wheat in Lebanon and Syria in 2010–2011. Plant Pathology. 2020;69(4):618-630. DOI: 10.1111/ppa.13164

5. Fontyn C., Zippert A.C., Delestre G., Marcel T.C., Suffert F., Goyeau H. Is virulence phenotype evolution driven exclusively by Lr gene deployment in French Puccinia triticina populations? Plant Pathology. 2022;71(7):1511-1524. DOI: 10.1111/ppa.13599

6. Gassner G., Straib W. Untersuchungen über die Infektionsbedingungen von Puccinia glumarum und Puccinia graminis. Arbeitsergebnissen der Biologischen Reichsanstalt für Landund Forstwirtschaft. 1929;16(4):609-629. [in German]

7. GRRC. Global Rust Reference Center. Stem and yellow rust genotyping and race analyses: [website]. Available from: https://agro.au.dk/forskning/internationale-platforme/wheatrust [accessed Mar. 01, 2023].

8. Gultyaeva E.I., Shaydayuk E.L. Virulence of Russian populations of the stripe rust causal agent. Mycology and Phytopathology. 2020;54(4):299-304. [in Russian]. DOI: 10.31857/S0026364820040042

9. Gultyaeva E.L., Shaydayuk E.L., Abdullaev K.M. Population genetics study of the wheat leaf rust agent Puccinia triticina in Dagestan. Proceedings of Applied Botany, Genetics and Breeding. 2018;179(2):140-150. [in Russian]. DOI: 10.30901/2227-8834-2018-2-140-150

10. Hasanova G.M., Rustamov Kh.N. Influence of yellow rust on quality indicators of bread wheat grain (T. aestivum L.). Agrarian Science. 2019;(1):158-161. [in Russian]. DOI: 10.32634/0869-8155-2019-326-1-158-161

11. Hovmøller M.S., Walter S., Bayles R.A., Hubbard A., Flath K., Sommerfeldt N. et al. Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathology. 2016;65(3):402-411. DOI: 10.1111/ppa.12433

12. Justesen A.F., Ridout C.J., Hovmøller M.S. The recent history of Puccinia striiformis f. sp. tritici in Denmark as revealed by disease incidence and AFLP markers. Plant Pathology. 2002;51(1):13-23. DOI: 10.1046/j.0032-0862.2001.00651.x

13. McIntosh R.A., Wellings C.R., Park R.F. (eds). Wheat rusts. An atlas of resistance genes. Dordrecht: Springer Netherlands; 1995.

14. Mikhailova L.A., Abdullaev K.M., Shelomova L.F. Shifts of Puccinia recondita Rob. ex Desm. f. sp. tritici population structure in Derbent environs (Daghestan) during 1970–1995. Mycology and Phytopathology. 1997;31(2):71-77. [in Russian]

15. Mikhailova L.A., Gultyaeva E.I., Mironenko N.V. Methods for studying the structure of populations of the leaf rust causative agent (Metody issledovaniy struktury populyatsii vozbuditelya buroy rzhavchiny pshenitsy). In: Collection of Plant Protection Guidelines (Sbornik metodicheskikh rekomendatsiy po zashchite rasteniy). St. Petersburg: VIZR; 1998. p.105-126. [in Russian]

16. Milus E.A., Kristensen K., Hovmøller M.S. Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology. 2009;99(1):89-94. DOI: 10.1094/PHYTO-99-1-0089 RustTracker.org. A Global Wheat Rust Monitoring System: [website]. Available from: https://rusttracker.cimmyt.org [accessed Mar. 01, 2023].

17. Sharma-Poudyal D., Chen X.M., Wan A.M., Zhan G.M., Kang Z.S., Cao S.Q. et al. Virulence characterization of international collections of the wheat stripe rust pathogen, Puccinia striiformis f. sp. tritici. Plant Disease. 2013;97(3):379-386. DOI: 10.1094/pdis-01-12-0078-re

18. Shaydayuk E.L., Yakovleva D.R., Abdullaev K.M., Pyukkenen V.P., Gultyaeva E.I. Population genetics studies of Puccinia striiformis f. sp. tritici in Dagestan and Northwestern Russia. Proceedings on Applied Botany, Genetics and Breeding. 2021;182(3):174-181. [in Russian]. DOI: 10.30901/2227-8834-2021-3-174-181

19. Sinha P., Chen X. Potential infection risks of the wheat stripe rust and stem rust pathogens on barberry in Asia and Southeastern Europe. Plants. 2021;10(5):957. DOI: 10.3390/plants10050957

20. Walter S., Ali S., Kemen E., Nazari K., Bahri B.A., Enjalbert J. et al. Molecular markers for tracking the origin and worldwide distribution of invasive strains of Puccinia striiformis. Ecology and Evolution. 2016;6(9):2790-2804. DOI: 10.1002/ece3.2069

21. Wan A.M., Chen X.M., Yuen J. Races of Puccinia striiformis f. sp. tritici in the United States in 2011 and 2012 and comparison with races in 2010. Plant Disease. 2016;100(5):966-975. DOI: 10.1094/PDIS-10-15-1122-RE

22. Wang M.N., Chen X.M. First report of Oregon grape (Mahonia aquifolium) as an alternate host for the wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici) under artificial inoculation. Plant Disease. 2013;97(6):839. DOI: 10.1094/PDIS-09-12-0864-PDN

23. Wellings C.R. Puccinia striiformis in Australia: a review of the incursion, evolution and adaptation of stripe rust in the period 1979–2006. Australian Journal of Agricultural Research. 2007;58(6):567-575. DOI: 10.1071/AR07130

24. Zhao J., Wang L., Wang Z., Chen X., Zhang H., Yao J. et al. Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology. 2013;103(9):927-934. DOI: 10.1094/PHYTO-09-12-0249-R