The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein

Qiuhong Wu; Yu Cui; Xuejiao Jin; Guoxin Wang; Lijie Yan; Chenchen Zhong; Meihua Yu; Wenli Li; Yong Wang; Ling Wang; Hao Wang; Chen Dang; Xinyu Zhang; Yongxing Chen; Panpan Zhang; Xiaofei Zhao; Jiajie Wu; Daolin Fu; Lanqin Xia; Eviatar Nevo; John Vogel; Naxin Huo; Dawei Li; Yong Q. Gu; Andrew O. Jackson; Yongliang Zhang; Zhiyong Liu

doi:10.1111/nph.18457

The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein

Qiuhong Wu, Yu Cui, Xuejiao Jin, Guoxin Wang, Lijie Yan, Chenchen Zhong, Meihua Yu, Wenli Li, Yong Wang, Ling Wang, Hao Wang, Chen Dang, Xinyu Zhang, Yongxing Chen, Panpan Zhang, Xiaofei Zhao, Jiajie Wu, Daolin Fu, Lanqin Xia, Eviatar NevoJohn Vogel, Naxin Huo, Dawei Li, Yong Q. Gu, Andrew O. Jackson, Yongliang Zhang, Zhiyong Liu

Department of Evolutionary and Environmental Biology

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

Abstract

Although some nucleotide binding, leucine-rich repeat immune receptor (NLR) proteins conferring resistance to specific viruses have been identified in dicot plants, NLR proteins involved in viral resistance have not been described in monocots. We have used map-based cloning to isolate the CC-NB-LRR (CNL) Barley stripe mosaic virus (BSMV) resistance gene barley stripe resistance 1 (BSR1) from Brachypodium distachyon Bd3-1 inbred line. Stable BSR1 transgenic Brachypodium line Bd21-3, barley (Golden Promise) and wheat (Kenong 199) plants developed resistance against BSMV ND18 strain. Allelic variation analyses indicated that BSR1 is present in several Brachypodium accessions collected from countries in the Middle East. Protein domain swaps revealed that the intact LRR domain and the C-terminus of BSR1 are required for resistance. BSR1 interacts with the BSMV ND18 TGB1 protein in planta and shows temperature-sensitive antiviral resistance. The R³⁹⁰ and T³⁹² residues of TGB1_ND (ND18 strain) and the G¹⁹⁶ and K¹⁹⁷ residues within the BSR1 P-loop motif are key amino acids required for immune activation. BSR1 is the first cloned virus resistance gene encoding a typical CNL protein in monocots, highlighting the utility of the Brachypodium model for isolation and analysis of agronomically important genes for crop improvement.

Original language	English
Journal	New Phytologist
DOIs	https://doi.org/10.1111/nph.18457
State	Accepted/In press - 2022

Bibliographical note

Funding Information:
We would like to thank Drs Jialin Yu, Chenggui Han and Xian‐Bing Wang at China Agricultural University for their helpful comments. This work was supported by the National Key Research and Development Program of China (2021YFA1300703 to ZL), the National Natural Science Foundation of China (32122070 and 31872637 to YZ).

Publisher Copyright:
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

Keywords

Barley stripe mosaic virus (BSMV)
Brachypodium
BSR1
gene-for-gene interaction
triple gene block 1 (TGB1)

ASJC Scopus subject areas

Physiology
Plant Science

Access to Document

10.1111/nph.18457

Cite this

Wu, Q., Cui, Y., Jin, X., Wang, G., Yan, L., Zhong, C., Yu, M., Li, W., Wang, Y., Wang, L., Wang, H., Dang, C., Zhang, X., Chen, Y., Zhang, P., Zhao, X., Wu, J., Fu, D., Xia, L., ... Liu, Z. (Accepted/In press). The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein. New Phytologist. https://doi.org/10.1111/nph.18457

@article{c771aaa11d0f4d95a78d7e12e59e1e3f,

title = "The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein",

abstract = "Although some nucleotide binding, leucine-rich repeat immune receptor (NLR) proteins conferring resistance to specific viruses have been identified in dicot plants, NLR proteins involved in viral resistance have not been described in monocots. We have used map-based cloning to isolate the CC-NB-LRR (CNL) Barley stripe mosaic virus (BSMV) resistance gene barley stripe resistance 1 (BSR1) from Brachypodium distachyon Bd3-1 inbred line. Stable BSR1 transgenic Brachypodium line Bd21-3, barley (Golden Promise) and wheat (Kenong 199) plants developed resistance against BSMV ND18 strain. Allelic variation analyses indicated that BSR1 is present in several Brachypodium accessions collected from countries in the Middle East. Protein domain swaps revealed that the intact LRR domain and the C-terminus of BSR1 are required for resistance. BSR1 interacts with the BSMV ND18 TGB1 protein in planta and shows temperature-sensitive antiviral resistance. The R390 and T392 residues of TGB1ND (ND18 strain) and the G196 and K197 residues within the BSR1 P-loop motif are key amino acids required for immune activation. BSR1 is the first cloned virus resistance gene encoding a typical CNL protein in monocots, highlighting the utility of the Brachypodium model for isolation and analysis of agronomically important genes for crop improvement.",

keywords = "Barley stripe mosaic virus (BSMV), Brachypodium, BSR1, gene-for-gene interaction, triple gene block 1 (TGB1)",

author = "Qiuhong Wu and Yu Cui and Xuejiao Jin and Guoxin Wang and Lijie Yan and Chenchen Zhong and Meihua Yu and Wenli Li and Yong Wang and Ling Wang and Hao Wang and Chen Dang and Xinyu Zhang and Yongxing Chen and Panpan Zhang and Xiaofei Zhao and Jiajie Wu and Daolin Fu and Lanqin Xia and Eviatar Nevo and John Vogel and Naxin Huo and Dawei Li and Gu, {Yong Q.} and Jackson, {Andrew O.} and Yongliang Zhang and Zhiyong Liu",

note = "Funding Information: We would like to thank Drs Jialin Yu, Chenggui Han and Xian‐Bing Wang at China Agricultural University for their helpful comments. This work was supported by the National Key Research and Development Program of China (2021YFA1300703 to ZL), the National Natural Science Foundation of China (32122070 and 31872637 to YZ). Publisher Copyright: {\textcopyright} 2022 The Authors. New Phytologist {\textcopyright} 2022 New Phytologist Foundation. This article has been contributed to by US Government employees and their work is in the public domain in the USA.",

year = "2022",

doi = "10.1111/nph.18457",

language = "English",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

}

Wu, Q, Cui, Y, Jin, X, Wang, G, Yan, L, Zhong, C, Yu, M, Li, W, Wang, Y, Wang, L, Wang, H, Dang, C, Zhang, X, Chen, Y, Zhang, P, Zhao, X, Wu, J, Fu, D, Xia, L, Nevo, E, Vogel, J, Huo, N, Li, D, Gu, YQ, Jackson, AO, Zhang, Y & Liu, Z 2022, 'The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein', New Phytologist. https://doi.org/10.1111/nph.18457

TY - JOUR

T1 - The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein

AU - Wu, Qiuhong

AU - Cui, Yu

AU - Jin, Xuejiao

AU - Wang, Guoxin

AU - Yan, Lijie

AU - Zhong, Chenchen

AU - Yu, Meihua

AU - Li, Wenli

AU - Wang, Yong

AU - Wang, Ling

AU - Wang, Hao

AU - Dang, Chen

AU - Zhang, Xinyu

AU - Chen, Yongxing

AU - Zhang, Panpan

AU - Zhao, Xiaofei

AU - Wu, Jiajie

AU - Fu, Daolin

AU - Xia, Lanqin

AU - Nevo, Eviatar

AU - Vogel, John

AU - Huo, Naxin

AU - Li, Dawei

AU - Gu, Yong Q.

AU - Jackson, Andrew O.

AU - Zhang, Yongliang

AU - Liu, Zhiyong

N1 - Funding Information: We would like to thank Drs Jialin Yu, Chenggui Han and Xian‐Bing Wang at China Agricultural University for their helpful comments. This work was supported by the National Key Research and Development Program of China (2021YFA1300703 to ZL), the National Natural Science Foundation of China (32122070 and 31872637 to YZ). Publisher Copyright: © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

PY - 2022

Y1 - 2022

N2 - Although some nucleotide binding, leucine-rich repeat immune receptor (NLR) proteins conferring resistance to specific viruses have been identified in dicot plants, NLR proteins involved in viral resistance have not been described in monocots. We have used map-based cloning to isolate the CC-NB-LRR (CNL) Barley stripe mosaic virus (BSMV) resistance gene barley stripe resistance 1 (BSR1) from Brachypodium distachyon Bd3-1 inbred line. Stable BSR1 transgenic Brachypodium line Bd21-3, barley (Golden Promise) and wheat (Kenong 199) plants developed resistance against BSMV ND18 strain. Allelic variation analyses indicated that BSR1 is present in several Brachypodium accessions collected from countries in the Middle East. Protein domain swaps revealed that the intact LRR domain and the C-terminus of BSR1 are required for resistance. BSR1 interacts with the BSMV ND18 TGB1 protein in planta and shows temperature-sensitive antiviral resistance. The R390 and T392 residues of TGB1ND (ND18 strain) and the G196 and K197 residues within the BSR1 P-loop motif are key amino acids required for immune activation. BSR1 is the first cloned virus resistance gene encoding a typical CNL protein in monocots, highlighting the utility of the Brachypodium model for isolation and analysis of agronomically important genes for crop improvement.

AB - Although some nucleotide binding, leucine-rich repeat immune receptor (NLR) proteins conferring resistance to specific viruses have been identified in dicot plants, NLR proteins involved in viral resistance have not been described in monocots. We have used map-based cloning to isolate the CC-NB-LRR (CNL) Barley stripe mosaic virus (BSMV) resistance gene barley stripe resistance 1 (BSR1) from Brachypodium distachyon Bd3-1 inbred line. Stable BSR1 transgenic Brachypodium line Bd21-3, barley (Golden Promise) and wheat (Kenong 199) plants developed resistance against BSMV ND18 strain. Allelic variation analyses indicated that BSR1 is present in several Brachypodium accessions collected from countries in the Middle East. Protein domain swaps revealed that the intact LRR domain and the C-terminus of BSR1 are required for resistance. BSR1 interacts with the BSMV ND18 TGB1 protein in planta and shows temperature-sensitive antiviral resistance. The R390 and T392 residues of TGB1ND (ND18 strain) and the G196 and K197 residues within the BSR1 P-loop motif are key amino acids required for immune activation. BSR1 is the first cloned virus resistance gene encoding a typical CNL protein in monocots, highlighting the utility of the Brachypodium model for isolation and analysis of agronomically important genes for crop improvement.

KW - Barley stripe mosaic virus (BSMV)

KW - Brachypodium

KW - BSR1

KW - gene-for-gene interaction

KW - triple gene block 1 (TGB1)

UR - http://www.scopus.com/inward/record.url?scp=85138284601&partnerID=8YFLogxK

U2 - 10.1111/nph.18457

DO - 10.1111/nph.18457

M3 - Article

AN - SCOPUS:85138284601

SN - 0028-646X

JO - New Phytologist

JF - New Phytologist

ER -

The CC–NB–LRR protein BSR1 from Brachypodium confers resistance to Barley stripe mosaic virus in gramineous plants by recognising TGB1 movement protein

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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