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Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties

The soil-borne yellow mosaic virus disease, which is caused by the bymoviruses barley yellow mosaic virus (BaYMV) and/or barley mild mosaic virus (BaMMV), seriously threatens winter barley production in Europe and East Asia. Both viruses are transmitted by the soil-borne plasmodiophorid Polymyxa gra...

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Autores principales: Cheng, Chunyuan, Kan, Jinhong, Li, Shanshan, Jiang, Congcong, He, Xiaoyan, Shen, Huiquan, Xu, Rugen, Li, Boqun, Feng, Zongyun, Yang, Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9583009/
https://www.ncbi.nlm.nih.gov/pubmed/36275526
http://dx.doi.org/10.3389/fpls.2022.1018379
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author Cheng, Chunyuan
Kan, Jinhong
Li, Shanshan
Jiang, Congcong
He, Xiaoyan
Shen, Huiquan
Xu, Rugen
Li, Boqun
Feng, Zongyun
Yang, Ping
author_facet Cheng, Chunyuan
Kan, Jinhong
Li, Shanshan
Jiang, Congcong
He, Xiaoyan
Shen, Huiquan
Xu, Rugen
Li, Boqun
Feng, Zongyun
Yang, Ping
author_sort Cheng, Chunyuan
collection PubMed
description The soil-borne yellow mosaic virus disease, which is caused by the bymoviruses barley yellow mosaic virus (BaYMV) and/or barley mild mosaic virus (BaMMV), seriously threatens winter barley production in Europe and East Asia. Both viruses are transmitted by the soil-borne plasmodiophorid Polymyxa graminis and are difficult to eliminate through chemical or physical measures in the field, making breeding for resistant cultivars the optimal strategy for disease control. The resistance locus rym1/11 was cloned encoding the host factor gene Protein Disulfide Isomerase Like 5-1 (PDIL5-1), whose loss-of-function variants confer broad-spectrum resistance to multiple strains of BaMMV/BaYMV. Most resistance-conferring variants have been identified in six-rowed barley landraces/historic cultivars, and their introgression into modern two-rowed malting cultivars is difficult because PDIL5-1 is located in a peri-centromeric region with suppressed recombination. In this study, we used CRISPR/Cas9 genome editing to modify PDIL5-1 in the BaYMV/BaMMV-susceptible elite malting barley cv. ‘Golden Promise’ and obtained the mutants pdil5-1-a and pdil5-1-b. PDIL5-1 in the pdil5-1-a mutant encodes a protein lacking a cysteine residue, and pdil5-1-b contains a protein-coding frameshift. Both mutants were completely resistant to BaYMV. The knockout mutant pdil5-1-b showed complete BaMMV resistance, while pdil5-1-a showed decreased viral accumulation but no disease symptoms if compared to ‘Golden Promise’. Both PDIL5-1 edited lines, as well as the previously produced EMS-induced pdil5-1 mutant ‘10253-1-5’ in the elite malting barley cv. ‘Barke’ background, displayed no growth or yield penalties in garden experiments or bymovirus-free field trials. Line ‘10253-1-5’ showed improved resistance and yield performance compared to the wild-type and its sibling line when grown in infectious fields. Therefore, genome editing of the host factor gene PDIL5-1 could facilitate the breeding of barley varieties with resistance to bymoviruses.
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spelling pubmed-95830092022-10-21 Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties Cheng, Chunyuan Kan, Jinhong Li, Shanshan Jiang, Congcong He, Xiaoyan Shen, Huiquan Xu, Rugen Li, Boqun Feng, Zongyun Yang, Ping Front Plant Sci Plant Science The soil-borne yellow mosaic virus disease, which is caused by the bymoviruses barley yellow mosaic virus (BaYMV) and/or barley mild mosaic virus (BaMMV), seriously threatens winter barley production in Europe and East Asia. Both viruses are transmitted by the soil-borne plasmodiophorid Polymyxa graminis and are difficult to eliminate through chemical or physical measures in the field, making breeding for resistant cultivars the optimal strategy for disease control. The resistance locus rym1/11 was cloned encoding the host factor gene Protein Disulfide Isomerase Like 5-1 (PDIL5-1), whose loss-of-function variants confer broad-spectrum resistance to multiple strains of BaMMV/BaYMV. Most resistance-conferring variants have been identified in six-rowed barley landraces/historic cultivars, and their introgression into modern two-rowed malting cultivars is difficult because PDIL5-1 is located in a peri-centromeric region with suppressed recombination. In this study, we used CRISPR/Cas9 genome editing to modify PDIL5-1 in the BaYMV/BaMMV-susceptible elite malting barley cv. ‘Golden Promise’ and obtained the mutants pdil5-1-a and pdil5-1-b. PDIL5-1 in the pdil5-1-a mutant encodes a protein lacking a cysteine residue, and pdil5-1-b contains a protein-coding frameshift. Both mutants were completely resistant to BaYMV. The knockout mutant pdil5-1-b showed complete BaMMV resistance, while pdil5-1-a showed decreased viral accumulation but no disease symptoms if compared to ‘Golden Promise’. Both PDIL5-1 edited lines, as well as the previously produced EMS-induced pdil5-1 mutant ‘10253-1-5’ in the elite malting barley cv. ‘Barke’ background, displayed no growth or yield penalties in garden experiments or bymovirus-free field trials. Line ‘10253-1-5’ showed improved resistance and yield performance compared to the wild-type and its sibling line when grown in infectious fields. Therefore, genome editing of the host factor gene PDIL5-1 could facilitate the breeding of barley varieties with resistance to bymoviruses. Frontiers Media S.A. 2022-10-06 /pmc/articles/PMC9583009/ /pubmed/36275526 http://dx.doi.org/10.3389/fpls.2022.1018379 Text en Copyright © 2022 Cheng, Kan, Li, Jiang, He, Shen, Xu, Li, Feng and Yang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Cheng, Chunyuan
Kan, Jinhong
Li, Shanshan
Jiang, Congcong
He, Xiaoyan
Shen, Huiquan
Xu, Rugen
Li, Boqun
Feng, Zongyun
Yang, Ping
Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title_full Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title_fullStr Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title_full_unstemmed Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title_short Mutation of barley HvPDIL5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
title_sort mutation of barley hvpdil5-1 improves resistance to yellow mosaic virus disease without growth or yield penalties
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9583009/
https://www.ncbi.nlm.nih.gov/pubmed/36275526
http://dx.doi.org/10.3389/fpls.2022.1018379
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