Pan-genome analysis reveals a highly plastic genome and extensive secreted protein polymorphism in <i>Puccinia striiformis</i> f. sp. <i>tritici</i>

Jierong Wang; Yuxi Peng; Yiwen Xu; Zhiru Li; Gangming Zhan; Zhensheng Kang; Jing Zhao

doi:10.1016/j.jgg.2023.12.004

Volume 51 Issue 5

May 2024

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Pan-genome analysis reveals a highly plastic genome and extensive secreted protein polymorphism in Puccinia striiformis f. sp. tritici

doi: 10.1016/j.jgg.2023.12.004

1. College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China;
2. State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi 712100, China;
3. College of Life Science, Northwest A&F University, Yangling, Shaanxi 712100, China;
4. College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China;
5. College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China;
6. State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi 712100, China

Funds:

F University for providing computing resources. This work was supported by grants from the National Key Research and Development Program of China (2021YFD1401001), Shaanxi Province Postdoctoral Science Foundation (2023BSHEDZZ121), and the National “111 plan” of China (BP0719026).

F University and High-Performance Computing of State Key Laboratory of Crop Stress Biology for Arid Areas of Northwest A&

We thank Professor Yu Jiang for the assistance of the analyses in this study. We also thank Dr. Chongjing Xia for providing the virulence data of CYR34 on the Yr single-gene lines. We would like to acknowledge the High-Performance Computing of Northwest A&

Received Date: 2023-09-08
Available Online: 2025-06-06
Publish Date: 2023-12-20

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References

Chen, X., Kang, Z. 2017. Stripe rust. Springer Netherlands.

Chin, C., Peluso, P., Sedlazeck, F.J., Nattestad, M., Concepcion, G.T., Clum, A., Dunn, C., O'Malley, R., Figueroa-Balderas, R., Morales-Cruz, A., et al., 2016. Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050-1054.

Cuomo, C.A., Bakkeren, G., Khalil, H.B., Panwar, V., Joly, D., Linning, R., Sakthikumar, S., Song, X., Adiconis, X., Fan, L., et al., 2017. Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci. G3 7, 361-376.

Duan, H., Jones, A.W., Hewitt, T., Mackenzie, A., Hu, Y., Sharp, A., Lewis, D., Mago, R., Upadhyaya, N.M., Rathjen, J.P., et al., 2022. Physical separation of haplotypes in dikaryons allows benchmarking of phasing accuracy in Nanopore and HiFi assemblies with Hi-C data. Genome Biol. 23.

Fouche, S., Plissonneau, C., Croll, D., 2018. The birth and death of effectors in rapidly evolving filamentous pathogen genomes. Curr. Opin. Microbiol. 46, 34-42.

Gao, X., Zhao, J., Liu, B., Guo, Y., Kang, Z., and Zhan, G. 2023. Population genetic analysis of Puccinia striiformis tritici in main winter-increasing areas based on virulent phenotypes and genotypes. Scientia Agricultura Sinica 56:2629-2642.

Huang, J., Jia, Q.Z., Zhang, B., Sun, Z.Y., Huang, M.M., and Jin, S.L. 2018. Epidemic forecasting of the new strains G22-9 (CYR34) and G22-14 of Puccinia striiformis f. sp tritici in wheat in Gansu Province. Journal of Plant Protection 45:101-108.

Li, H., Durbin, R., 2024. Genome assembly in the telomere-to-telomere era. Nat. Rev. Genet. https://doi.org/10.1038/s41576-024-00718-w.

Li, Y., Xia, C., Wang, M., Yin, C., Chen, X., 2019. Genome sequence resource of a Puccinia striiformis isolate infecting wheatgrass. Phytopathology 109, 1509-1512.

Schwessinger, B., 2016. Fundamental wheat stripe rust research in the 21st century. New Phytol. 213, 1625-1631.

Schwessinger, B., Sperschneider, J., Cuddy, W.S., Garnica, D.P., Miller, M.E., Taylor, J.M., Dodds, P.N., Figuero, M., Park, R.F., Rathjen, J.P., 2018. A near-complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high interhaplotype diversity. mBio 9, e02275-17.

Schwessinger, B., Jones, A., Albekaa, M., Hu, Y., Mackenzie, A., Tam, R., Nagar, R., Milgate, A., Rathjen, J.P., Periyannan, S., 2022. A chromosome scale assembly of an Australian Puccinia striiformis f. sp. tritici isolate of the PstS1 lineage. Mol. Plant-Microbe Interact. 35, 293-296.

Schwessinger, B., Chen, Y., Tien, R., Vogt, J.K., Sperschneider, J., Nagar, R., McMullan, M., Sicheritz-Ponten, T., Soerensen, C.K., Hovmoeller, M.S., et al., 2020. Distinct life histories impact dikaryotic genome evolution in the rust fungus Puccinia striiformis causing stripe rust in wheat. Genome Biol. Evol. 12, 597-617.

Toruno, T.Y., Stergiopoulos, I., Coaker, G., 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54, 419-441.

Vasquez-Gross, H., Kaur, S., Epstein, L., Dubcovsky, J., 2020. A haplotype-phased genome of wheat stripe rust pathogen Puccinia striiformis f. sp. tritici, race PST-130 from the western USA. PLoS One 15, e0238611.

Wang, J., Zhan, G., Tian, Y., Zhang, Y., Xu, Y., Kang, Z., Zhao, J., 2022. Role of sexual reproduction in the evolution of the wheat stripe rust fungus races in China. Phytopathology 112, 1063-1071.

Xia, C., Huang, L., Huang, J., Zhang, H., Huang, Y., Benhamed, M., Wang, M., Chen, X., Zhang, M., Liu, T., et al., 2022. Folding features and dynamics of 3D genome architecture in plant fungal pathogens. Microbiol. Spectr. 10, e0260822.

Zhao, J., Kang, Z., 2023. Fighting wheat rusts in China: a look back and into the future. Phytopathol. Res. 5, 1-30.

Zhao, J., Wang, M., Chen, X., Kang, Z., 2016. Role of alternate hosts in epidemiology and pathogen variation of cereal rusts. Annu. Rev. Phytopathol. 54, 207-228.

Zheng, W., Huang, L., Huang, J., Wang, X., Chen, X., Zhao, J., Guo, J., Zhuang, H., Qiu, C., Liu, J., et al., 2013. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat. Commun. 4, 2673.

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1.	Guan, H., Zhang, P., Park, R.F. et al. Genomics Research on the Road of Studying Biology and Virulence of Cereal Rust Fungi. Molecular Plant Pathology, 2025, 26(4): e70082.
2.	Ma, X., Kang, Z., Zhang, Z. et al. Secreted Xylanase PstXyn1 Contributes to Stripe Rust Infection Possibly by Overcoming Cell Wall Barrier and Suppressing Defense Responses in Wheat. Journal of Agricultural and Food Chemistry, 2025, 73(1): 380–392.
3.	Cerav, E.N., Wu, N., Akkaya, M.S. Transcriptome-Wide N6-Methyladenosine (m6A) Methylation Analyses in a Compatible Wheat–Puccinia striiformis f. sp. tritici Interaction. Plants, 2024, 13(7): 982.