Extensive genetic variation at the Sr22 wheat stem rust resistance gene locus in the grasses revealed through evolutionary genomics and functional analyses

Authors: HATTA, ASYRAF - John Innes Center; GHOSH, SREYA - John Innes Center; ATHIYANNAN, NAVEENKUMAR - Commonwealth Scientific And Industrial Research Organisation (CSIRO); RICHARDSON, TERESE - Commonwealth Scientific And Industrial Research Organisation (CSIRO); STEUERNAGEL, BURKHARD - John Innes Center; YU, GUOTAI - John Innes Center; Rouse, Matthew - Matt; AYLIFFE, MICK - Commonwealth Scientific And Industrial Research Organisation (CSIRO); LAGUDAH, EVANS - Commonwealth Scientific And Industrial Research Organisation (CSIRO); RADHAKRISHNAN, GURU - John Innes Center; PERIYANNAN, SAMBASIVAM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); WULFF, BRANDE - John Innes Center

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/7/2020
Publication Date: 10/1/2020
Citation: Hatta, A.M., Ghosh, S., Athiyannan, N., Richardson, T., Steuernagel, B., Yu, G., Rouse, M.N., Ayliffe, M., Lagudah, E.S., Radhakrishnan, G.V., Periyannan, S.K., Wulff, B.B. 2020. Extensive genetic variation at the Sr22 wheat stem rust resistance gene locus in the grasses revealed through evolutionary genomics and functional analyses. Molecular Plant-Microbe Interactions. 33(11):1286-1298. https://doi.org/10.1094/MPMI-01-20-0018-R.
DOI: https://doi.org/10.1094/MPMI-01-20-0018-R

Interpretive Summary: In the last 20 years, severe wheat stem rust outbreaks have been recorded in Africa, Europe and Central Asia. This previously well controlled disease has re-emerged as a major threat to wheat cultivation. The stem rust (Sr) resistance gene Sr22 confers resistance to the highly virulent African stem rust isolate Ug99. Here, we describe fourteen Sr22 homolog sequence variants obtained from wild relatives of wheat, which have been postulated to encode both functional and non-functional Sr22 alleles. Three Sr22 homologs were transformed into wheat cv. Fielder and two were resistant to Ug99, thereby unequivocally confirming Sr22 effectiveness against Ug99. The third Sr22 homolog, previously believed to confer susceptibility, was confirmed as non-functional against an Australian stem rust pathogen race. This information is valuable for informing the utilization of Sr22 by various means in wheat cultivars. Ug99-resistant wheat cultivars can protect United States wheat production from devastating stem rust epidemics, if Ug99 or other virulent races of the stem rust pathogen establish in the United States.

Technical Abstract: In the last 20 years, severe wheat stem rust outbreaks have been recorded in Africa, Europe and Central Asia. This previously well controlled disease, caused by the fungus Puccinia graminis f. sp. tritici (Pgt), has re-emerged as a major threat to wheat cultivation. The stem rust (Sr) resistance gene Sr22 encodes a nucleotide-binding and leucine-rich repeat (NLR) receptor which confers resistance to the highly virulent African stem rust isolate Ug99. Here, we show that Triticeae species contain syntenic loci with single-copy orthologs of Sr22 on chromosome 7 except Hordeum vulgare which has experienced major expansions and rearrangements at the locus. We also describe fourteen Sr22 sequence variants obtained from both Triticum boeoticum and the domesticated form of this species, Triticum monococcum, which have been postulated to encode both functional and non-functional Sr22 alleles. The nucleotide sequence analysis of these alleles identified historical sequence exchange including breakpoints within codons which expanded the coding potential at these positions by introduction of non-synonymous substitutions. As an alternative to native regulatory sequences, Sr33 5' and 3' regulatory elements were used for rapid functional testing of Sr22 alleles. Three Sr22 alleles were transformed into wheat cv. Fielder and two postulated resistant alleles from Schomburgk (hexaploid wheat introgressed with T. boeoticum segment carrying Sr22) and T. monococcum accession PI190945, respectively, conferred resistance to Pgt race TTKSK, thereby unequivocally confirming Sr22 effectiveness against Ug99. The third allele from accession PI573523, previously believed to confer susceptibility, was confirmed as non-functional against Australian Pgt race 98-1,2,3,5,6.