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

Baljeet K. Gill; Daryl L. Klindworth; Matthew N. Rouse; Jinglun Zhang; Qijun Zhang; Jyoti S. Sharma; Chenggen Chu; Yunming Long; Shiaoman Chao; Pablo D. Olivera; Timothy L. Friesen; Shaobin Zhong; Yue Jin; Justin D. Faris; Jason D. Fiedler; Elias M. Elias; Shuyu Liu; Xiwen Cai; Steven S. Xu

doi:10.1111/tpj.15263

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

Baljeet K. Gill, Daryl L. Klindworth, Matthew N. Rouse, Jinglun Zhang, Qijun Zhang, Jyoti S. Sharma, Chenggen Chu, Yunming Long, Shiaoman Chao, Pablo D. Olivera, Timothy L. Friesen, Shaobin Zhong, Yue Jin, Justin D. Faris, Jason D. Fiedler, Elias M. Elias, Shuyu Liu, Xiwen Cai, Steven S. Xu

Plant Pathology

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

14 Scopus citations

Abstract

The 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 has haplotypes R1, R2 and R3. The R1/R3 and R2 haplotypes were originally designated as alleles Sr13a and Sr13b, respectively. To detect additional Sr13 alleles, we developed Kompetitive allele specific PCR (KASP™) marker KASPSr13 and four semi-thermal asymmetric reverse PCR markers, rwgsnp37–rwgsnp40, based on the CNL13 sequence. These markers were shown to detect R1, R2 and R3 haplotypes in a panel of diverse tetraploid wheat accessions. 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 leucine-rich repeat region and differed from the other three R haplotypes by one or two 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, with the other three R alleles probably being derived from Sr13d through one or two additional point mutations.

Original language	English (US)
Pages (from-to)	1674-1691
Number of pages	18
Journal	Plant Journal
Volume	106
Issue number	6
DOIs	https://doi.org/10.1111/tpj.15263
State	Published - Jun 2021

Bibliographical note

Funding Information:
The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the gene sequence before publication to facilitate the development of the assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA‐ARS CRIS project no. 3060‐21000‐038‐00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer. Sr13 KASPSr13

Funding Information:
The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the Sr13 gene sequence before publication to facilitate the development of the KASPSr13 assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA-ARS CRIS project no. 3060-21000-038-00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer.

Publisher Copyright:
© 2021 Society for Experimental Biology and John Wiley & Sons Ltd

Keywords

Puccinia graminis f. sp. tritici
Sr13 alleles
Triticum turgidum
Ug99
stem rust
tetraploid wheat

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Gill, B. K., Klindworth, D. L., Rouse, M. N., Zhang, J., Zhang, Q., Sharma, J. S., Chu, C., 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 variations of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.). Plant Journal, 106(6), 1674-1691. https://doi.org/10.1111/tpj.15263

Gill, BK, Klindworth, DL, Rouse, MN, Zhang, J, Zhang, Q, Sharma, JS, Chu, C, Long, Y, Chao, S, Olivera, PD, Friesen, TL, Zhong, S, Jin, Y, Faris, JD, Fiedler, JD, Elias, EM, Liu, S, Cai, X & Xu, SS 2021, 'Function and evolution of allelic variations of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.)', Plant Journal, vol. 106, no. 6, pp. 1674-1691. https://doi.org/10.1111/tpj.15263

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title = "Function and evolution of allelic variations of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.)",

abstract = "The 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 has haplotypes R1, R2 and R3. The R1/R3 and R2 haplotypes were originally designated as alleles Sr13a and Sr13b, respectively. To detect additional Sr13 alleles, we developed Kompetitive allele specific PCR (KASP{\texttrademark}) marker KASPSr13 and four semi-thermal asymmetric reverse PCR markers, rwgsnp37–rwgsnp40, based on the CNL13 sequence. These markers were shown to detect R1, R2 and R3 haplotypes in a panel of diverse tetraploid wheat accessions. 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 leucine-rich repeat region and differed from the other three R haplotypes by one or two 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, with the other three R alleles probably being derived from Sr13d through one or two additional point mutations.",

keywords = "Puccinia graminis f. sp. tritici, Sr13 alleles, Triticum turgidum, Ug99, stem rust, tetraploid wheat",

author = "Gill, {Baljeet K.} and Klindworth, {Daryl L.} and Rouse, {Matthew N.} and Jinglun Zhang and Qijun Zhang and Sharma, {Jyoti S.} and Chenggen Chu and Yunming Long and Shiaoman Chao and Olivera, {Pablo D.} and Friesen, {Timothy L.} and Shaobin Zhong and Yue Jin and Faris, {Justin D.} and Fiedler, {Jason D.} and Elias, {Elias M.} and Shuyu Liu and Xiwen Cai and Xu, {Steven S.}",

note = "Funding Information: The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the gene sequence before publication to facilitate the development of the assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA‐ARS CRIS project no. 3060‐21000‐038‐00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer. Sr13 KASPSr13 Funding Information: The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the Sr13 gene sequence before publication to facilitate the development of the KASPSr13 assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA-ARS CRIS project no. 3060-21000-038-00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer. Publisher Copyright: {\textcopyright} 2021 Society for Experimental Biology and John Wiley & Sons Ltd",

year = "2021",

month = jun,

doi = "10.1111/tpj.15263",

language = "English (US)",

volume = "106",

pages = "1674--1691",

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T1 - Function and evolution of allelic variations of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.)

AU - Gill, Baljeet K.

AU - Klindworth, Daryl L.

AU - Rouse, Matthew N.

AU - Zhang, Jinglun

AU - Zhang, Qijun

AU - Sharma, Jyoti S.

AU - Chu, Chenggen

AU - Long, Yunming

AU - Chao, Shiaoman

AU - Olivera, Pablo D.

AU - Friesen, Timothy L.

AU - Zhong, Shaobin

AU - Jin, Yue

AU - Faris, Justin D.

AU - Fiedler, Jason D.

AU - Elias, Elias M.

AU - Liu, Shuyu

AU - Cai, Xiwen

AU - Xu, Steven S.

N1 - Funding Information: The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the gene sequence before publication to facilitate the development of the assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA‐ARS CRIS project no. 3060‐21000‐038‐00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer. Sr13 KASPSr13 Funding Information: The authors thank Mary Osenga and Danielle Holmes for technical support and assistance in genotyping and stem rust evaluations, respectively. We thank Dr Jorge Dubcovsky at the University of California, Davis for sharing the Sr13 gene sequence before publication to facilitate the development of the KASPSr13 assay and for providing transgenic and mutant lines. We thank Dr Robert McIntosh for his critical reading of the manuscript. This research was supported in part by funds to SSX provided through a grant from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance in Wheat (DRRW) Project and the USDA-ARS CRIS project no. 3060-21000-038-00D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. The US Department of Agriculture is an equal opportunity provider and employer. Publisher Copyright: © 2021 Society for Experimental Biology and John Wiley & Sons Ltd

PY - 2021/6

Y1 - 2021/6

N2 - The 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 has haplotypes R1, R2 and R3. The R1/R3 and R2 haplotypes were originally designated as alleles Sr13a and Sr13b, respectively. To detect additional Sr13 alleles, we developed Kompetitive allele specific PCR (KASP™) marker KASPSr13 and four semi-thermal asymmetric reverse PCR markers, rwgsnp37–rwgsnp40, based on the CNL13 sequence. These markers were shown to detect R1, R2 and R3 haplotypes in a panel of diverse tetraploid wheat accessions. 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 leucine-rich repeat region and differed from the other three R haplotypes by one or two 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, with the other three R alleles probably being derived from Sr13d through one or two additional point mutations.

AB - The 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 has haplotypes R1, R2 and R3. The R1/R3 and R2 haplotypes were originally designated as alleles Sr13a and Sr13b, respectively. To detect additional Sr13 alleles, we developed Kompetitive allele specific PCR (KASP™) marker KASPSr13 and four semi-thermal asymmetric reverse PCR markers, rwgsnp37–rwgsnp40, based on the CNL13 sequence. These markers were shown to detect R1, R2 and R3 haplotypes in a panel of diverse tetraploid wheat accessions. 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 leucine-rich repeat region and differed from the other three R haplotypes by one or two 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, with the other three R alleles probably being derived from Sr13d through one or two additional point mutations.

KW - Puccinia graminis f. sp. tritici

KW - Sr13 alleles

KW - Triticum turgidum

KW - Ug99

KW - stem rust

KW - tetraploid wheat

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

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