Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

Feng Li; Narayana M. Upadhyaya; Jana Sperschneider; Oadi Matny; Hoa Nguyen-Phuc; Rohit Mago; Castle Raley; Marisa E. Miller; Kevin A.T. Silverstein; Eva Henningsen; Cory D. Hirsch; Botma Visser; Zacharias A. Pretorius; Brian J. Steffenson; Benjamin Schwessinger; Peter N. Dodds; Melania Figueroa

doi:10.1038/s41467-019-12927-7

Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

Feng Li, Narayana M. Upadhyaya, Jana Sperschneider, Oadi Matny, Hoa Nguyen-Phuc, Rohit Mago, Castle Raley, Marisa E. Miller, Kevin A.T. Silverstein, Eva Henningsen, Cory D. Hirsch, Botma Visser, Zacharias A. Pretorius, Brian J. Steffenson, Benjamin Schwessinger, Peter N. Dodds, Melania Figueroa

Research output: Contribution to journal › Article › peer-review

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Abstract

Parasexuality contributes to diversity and adaptive evolution of haploid (monokaryotic) fungi. However, non-sexual genetic exchange mechanisms are not defined in dikaryotic fungi (containing two distinct haploid nuclei). Newly emerged strains of the wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), such as Ug99, are a major threat to global food security. Here, we provide genomics-based evidence supporting that Ug99 arose by somatic hybridisation and nuclear exchange between dikaryons. Fully haplotype-resolved genome assembly and DNA proximity analysis reveal that Ug99 shares one haploid nucleus genotype with a much older African lineage of Pgt, with no recombination or chromosome reassortment. These findings indicate that nuclear exchange between dikaryotes can generate genetic diversity and facilitate the emergence of new lineages in asexual fungal populations.

Original language	English (US)
Article number	5068
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12927-7
State	Published - Dec 1 2019

Bibliographical note

Funding Information:
We thank J. Ellis, P. van Esse, G. Bakkeren, C. Aime and Y. Jin for valuable discussions, S. Dahl and N. Prenevost for technical support, J. Palmer for gene annotation troubleshooting, and the Minnesota Supercomputing Institute for computational resources. This research was funded by two independent grants from the 2 Blades foundation to P.N.D. and M.F., respectively, by a USDA-Agriculture and Food Research Initiative (AFRI) Competitive Grant (Proposal No. 2017-08221) to M.F, and University of Minnesota Lieberman-Okinow Endowment to B.J.S.; M.F. and M.E.M were supported by the University of Minnesota Experimental Station USDA-NIFA Hatch/Figueroa project MIN-22-G19 and an USDA-NIFA Postdoctoral Fellowship award (2017-67012-26117), respectively. B.S. is supported by an ARC Future Fellowship (FT180100024). J.S. is supported by an ARC DECRA Fellowship (DE190100066).

Publisher Copyright:
© 2019, Crown.

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Li, F., Upadhyaya, N. M., Sperschneider, J., Matny, O., Nguyen-Phuc, H., Mago, R., Raley, C., Miller, M. E., Silverstein, K. A. T., Henningsen, E., Hirsch, C. D., Visser, B., Pretorius, Z. A., Steffenson, B. J., Schwessinger, B., Dodds, P. N., & Figueroa, M. (2019). Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation. Nature communications, 10(1), Article 5068. https://doi.org/10.1038/s41467-019-12927-7

Li, F, Upadhyaya, NM, Sperschneider, J, Matny, O, Nguyen-Phuc, H, Mago, R, Raley, C, Miller, ME, Silverstein, KAT, Henningsen, E, Hirsch, CD, Visser, B, Pretorius, ZA, Steffenson, BJ, Schwessinger, B, Dodds, PN & Figueroa, M 2019, 'Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation', Nature communications, vol. 10, no. 1, 5068. https://doi.org/10.1038/s41467-019-12927-7

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abstract = "Parasexuality contributes to diversity and adaptive evolution of haploid (monokaryotic) fungi. However, non-sexual genetic exchange mechanisms are not defined in dikaryotic fungi (containing two distinct haploid nuclei). Newly emerged strains of the wheat stem rust pathogen, Puccinia graminis f. sp. tritici (Pgt), such as Ug99, are a major threat to global food security. Here, we provide genomics-based evidence supporting that Ug99 arose by somatic hybridisation and nuclear exchange between dikaryons. Fully haplotype-resolved genome assembly and DNA proximity analysis reveal that Ug99 shares one haploid nucleus genotype with a much older African lineage of Pgt, with no recombination or chromosome reassortment. These findings indicate that nuclear exchange between dikaryotes can generate genetic diversity and facilitate the emergence of new lineages in asexual fungal populations.",

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AU - Mago, Rohit

AU - Raley, Castle

AU - Miller, Marisa E.

AU - Silverstein, Kevin A.T.

AU - Henningsen, Eva

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Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation

Abstract

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