Function and evolution of allelic variation of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.)

Authors: GILL, BALJEET - North Dakota State University; Klindworth, Daryl; Rouse, Matthew; ZHANG, JINGLUN - North Dakota State University; ZHANG, QIJUN - North Dakota State University; SHARMA, JYOTI - North Dakota State University; Chu, Chenggen; LONG, YUNMING - North Dakota State University; Chao, Shiaoman; OLIVERA, PABLO - University Of Minnesota; Friesen, Timothy; ZHONG, SHAOBIN - North Dakota State University; Jin, Yue; Faris, Justin; Fiedler, Jason; ELIAS, ELIAS - North Dakota State University; LIU, SHUYU - Texas A&M Agrilife; Cai, Xiwen; Xu, Steven

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2021
Publication Date: 4/7/2021
Citation: Gill, B., Klindworth, D.L., Rouse, M.N., Zhang, J., Zhang, Q., Sharma, J.S., Chu, C.N., Long, Y., Chao, S., Olivera, P.D., Friesen, T.L., Zhong, S., Jin, Y., Faris, J.D., Fiedler, J.D., Elias, E.M., Liu, S., Cai, X., Xu, S.S. 2021. Function and evolution of allelic variation of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.). Plant Journal. 106:1674-1691. https://doi.org/10.1111/tpj.15263.
DOI: https://doi.org/10.1111/tpj.15263

Interpretive Summary: Stem rust is historically the most damaging disease in durum and bread wheat. The occurrence of new strains (e.g., Ug99) of the fungal pathogen causing stem rust outbreaks and epidemics in East Africa, Europe and Central Asia in the last two decades indicate that wheat stem rust is an emerging disease, posing a threat to wheat production worldwide. To identify stem rust resistance genes that are effective against new strains of stem rust pathogen, we conducted genetic and molecular analysis on the stem rust resistance genes in a set of lines consisting of durum and closely related species. Genetic analysis and stem rust tests indicated the presence of four forms (namely alleles) of Sr13, one of the most important genes in durum wheat for resistance to stem rust. In addition to two previously reported alleles (Sr13a and Sr13b), two new alleles were identified in this study and designated as Sr13c and Sr13d, respectively. Stem rust testing with multiple strains of the pathogen showed that Sr13c is the strongest allele with resistance to all strains and should be a preferred allele for breeding resistance to stem rust, whereas Sr13d should be avoided in breeding due to its susceptibility to Ug99. The molecular markers developed in this study are also useful tools for detecting these alleles in wheat lines and for selecting specific alleles in the development of better wheat cultivars.

Technical Abstract: Resistance gene Sr13 is one of the most important genes in durum wheat for controlling stem rust caused by Puccinia graminis f. sp. tritici (Pgt). The Sr13 functional gene CNL13 was recently shown to have haplotypes R1, R2, and R3. Based on reaction to Pgt race JRCQC, the resistant (R1/R3) and susceptible (R2) haplotypes were originally designated as Sr13a and Sr13b, respectively. To detect additional Sr13 alleles, we developed the KASP marker KASPSr13 and four STARP markers, rwgsnp37 through rwgsnp40, based on the cloned CNL13 sequence. KASPSr13 and rwgsnp37 are diagnostic for Sr13 and rwgsnp38, 39, and 40 are diagnostic for R2, R3, and R1, respectively. A panel of diverse tetraploid wheat accessions tested with the four markers detected R1 in durum line Rusty-Kl-B, R2 in Triticum turgidum subsp. carthlicum PI 387696 and T. turgidum subsp. polonicum CItr 14803, and R3 in durum lines ‘Langdon’ and Rusty-ST464-C1. We also observed the presence of Sr13 in durum line CAT-A1 although it lacked any of the known haplotypes. Sequence analysis revealed that CNL13 of CAT-A1 differed from the susceptible haplotype S1 by a single nucleotide (C2200T) in the LRR region and differed from the other three R haplotypes by 1 - 2 additional nucleotides, confirming that CAT-A1 carries a new (R4) haplotype. Stem rust tests on the monogenic, transgenic, and mutant lines showed that R1 differed from R3 in its susceptibility to races TCMJC and THTSC, whereas R4 differed from all other haplotypes for susceptibility to TTKSK, TPPKC and TCCJC. Based on these differences, we designate the R1, R3 and R4 haplotypes as alleles Sr13a, Sr13c and Sr13d, respectively. This study indicates that Sr13d may be the primitive functional allele originating from the S1 haplotype via a point mutation and the other three R alleles were likely derived from Sr13d through 1 - 2 additional point mutations.