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

New Phytol. 2022 Dec;236(6):2233-2248. doi: 10.1111/nph.18457. Epub 2022 Sep 19.

Authors

Qiuhong Wu^#¹, Yu Cui^#², Xuejiao Jin^#³, Guoxin Wang^#⁴, Lijie Yan^#⁵, Chenchen Zhong⁵, Meihua Yu⁵, Wenli Li⁵, Yong Wang⁶, Ling Wang⁷, Hao Wang⁵, Chen Dang⁵, Xinyu Zhang⁵, Yongxing Chen^{1

8}, Panpan Zhang^{1

8}, Xiaofei Zhao⁵, Jiajie Wu⁹, Daolin Fu⁹, Lanqin Xia², Eviatar Nevo¹⁰, John Vogel¹¹, Naxin Huo¹², Dawei Li⁵, Yong Q Gu¹², Andrew O Jackson¹³, Yongliang Zhang⁵, Zhiyong Liu^{1

8}

Affiliations

¹ State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Science, Beijing, 100101, China.
² Institute of Crop Sciences, Chinese Academy of Agriculture Sciences, Beijing, 100081, China.
³ State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.
⁴ Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.
⁵ State Key Laboratory of Agro-Biotechnology, China Agricultural University, Beijing, 100193, China.
⁶ Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.
⁷ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
⁸ College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China.
⁹ College of Agronomy, Shandong Agriculture University, Taian, 271018, China.
¹⁰ Institute of Evolution, Haifa University, Haifa, 31905, Israel.
¹¹ Joint Genome Institute, DOE, Walnut Creek, CA, 94598, USA.
¹² USDA-ARS Western Regional Research Center, Albany, CA, 94710, USA.
¹³ Department of Plant and Microbiology, University of California, Berkeley, CA, 94720, USA.

^# Contributed equally.

PMID: 36059081
DOI: 10.1111/nph.18457

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.

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

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brachypodium* / genetics
Hordeum* / genetics
Leucine-Rich Repeat Proteins
Protein Domains

Substances

Leucine-Rich Repeat Proteins

Supplementary concepts

Barley stripe mosaic virus

Associated data

RefSeq/OM687299
RefSeq/OM687300