Multiomics analysis reveals the molecular mechanisms underlying virulence in Rhizoctonia and jasmonic acid-mediated resistance in tartary buckwheat (Fagopyrum tataricum)
Multiomics analysis reveals the molecular mechanisms underlying virulence in Rhizoctonia and jasmonic acid-mediated resistance in tartary buckwheat (Fagopyrum tataricum)
Rhizoctonia solani is a devastating soil-borne pathogen that seriously threatens the cultivation of economically important crops. Multiple strains with a very broad host range have been identified, but only 1 (AG1-IA, which causes rice sheath blight disease) has been examined in detail. Here, we analyzed AG4-HGI 3 originally isolated from Tartary buckwheat (Fagopyrum tataricum), but with a host range comparable to AG1-IA. Genome comparison reveals abundant pathogenicity genes in this strain. We used multiomic approaches to improve the efficiency of screening for disease resistance genes. Transcriptomes of the plant–fungi interaction identified differentially expressed genes associated with virulence in Rhizoctonia and resistance in Tartary buckwheat. Integration with jasmonate-mediated transcriptome and metabolome changes revealed a negative regulator of jasmonate signaling, cytochrome P450 (FtCYP94C1), as increasing disease resistance probably via accumulation of resistance-related flavonoids. The integration of resistance data for 320 Tartary buckwheat accessions identified a gene homolog to aspartic proteinase (FtASP), with peak expression following R. solani inoculation. FtASP exhibits no proteinase activity but functions as an antibacterial peptide that slows fungal growth. This work reveals a potential mechanism behind pathogen virulence and host resistance, which should accelerate the molecular breeding of resistant varieties in economically essential crops.
2773-2798
He, Yuqi
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Zhang, Kaixuan
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Li, Shijuan
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Lu, Xiang
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Zhao, Hui
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Guan, Chaonan
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Huang, Xu
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Shi, Yaliang
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Kang, Zhen
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Fan, Yu
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Li, Wei
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Chen, Cheng
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Li, Guangsheng
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Long, Ou
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Chen, Yuanyuan
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Hu, Mang
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Cheng, Jianping
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Xu, Bingliang
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Chapman, Mark A.
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Georgiev, Milen I.
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Fernie, Alisdair R.
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Zhou, Meiliang
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2 August 2023
He, Yuqi
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Zhang, Kaixuan
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Li, Shijuan
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Lu, Xiang
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Zhao, Hui
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Guan, Chaonan
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Huang, Xu
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Shi, Yaliang
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Kang, Zhen
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Fan, Yu
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Li, Wei
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Chen, Cheng
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Li, Guangsheng
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Long, Ou
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Chen, Yuanyuan
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Hu, Mang
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Cheng, Jianping
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Xu, Bingliang
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Chapman, Mark A.
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Georgiev, Milen I.
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Fernie, Alisdair R.
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Zhou, Meiliang
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He, Yuqi, Zhang, Kaixuan, Li, Shijuan, Lu, Xiang, Zhao, Hui, Guan, Chaonan, Huang, Xu, Shi, Yaliang, Kang, Zhen, Fan, Yu, Li, Wei, Chen, Cheng, Li, Guangsheng, Long, Ou, Chen, Yuanyuan, Hu, Mang, Cheng, Jianping, Xu, Bingliang, Chapman, Mark A., Georgiev, Milen I., Fernie, Alisdair R. and Zhou, Meiliang
(2023)
Multiomics analysis reveals the molecular mechanisms underlying virulence in Rhizoctonia and jasmonic acid-mediated resistance in tartary buckwheat (Fagopyrum tataricum).
The Plant Cell, 35 (8), , [koad118].
(doi:10.1093/plcell/koad118).
Abstract
Rhizoctonia solani is a devastating soil-borne pathogen that seriously threatens the cultivation of economically important crops. Multiple strains with a very broad host range have been identified, but only 1 (AG1-IA, which causes rice sheath blight disease) has been examined in detail. Here, we analyzed AG4-HGI 3 originally isolated from Tartary buckwheat (Fagopyrum tataricum), but with a host range comparable to AG1-IA. Genome comparison reveals abundant pathogenicity genes in this strain. We used multiomic approaches to improve the efficiency of screening for disease resistance genes. Transcriptomes of the plant–fungi interaction identified differentially expressed genes associated with virulence in Rhizoctonia and resistance in Tartary buckwheat. Integration with jasmonate-mediated transcriptome and metabolome changes revealed a negative regulator of jasmonate signaling, cytochrome P450 (FtCYP94C1), as increasing disease resistance probably via accumulation of resistance-related flavonoids. The integration of resistance data for 320 Tartary buckwheat accessions identified a gene homolog to aspartic proteinase (FtASP), with peak expression following R. solani inoculation. FtASP exhibits no proteinase activity but functions as an antibacterial peptide that slows fungal growth. This work reveals a potential mechanism behind pathogen virulence and host resistance, which should accelerate the molecular breeding of resistant varieties in economically essential crops.
Text
PlantCellFinal
- Accepted Manuscript
More information
Accepted/In Press date: 7 April 2023
e-pub ahead of print date: 29 April 2023
Published date: 2 August 2023
Additional Information:
Funding Information:
This research was supported by National Natural Science Foundation of China (32161143005, 31901511, 31871536 and 31801427), the Project of Sanya Yazhou Bay Science and Technology City (SCKJ-JYRC-2022-22), the Youth Innovation Program of Chinese Academy of Agricultural Sciences (Y2022QC02), National Key R&D Program of China (2017YFE0117600, 2019YFD1000700/2019YFD1000701), European Union Horizon 2020 project Planta SYST (SGA-CSA No. 739582 under FPA No.664620) and China National Postdoctoral Program for Innovative Talents (BX20200377).
Publisher Copyright:
© American Society of Plant Biologists 2023. All rights reserved.
Identifiers
Local EPrints ID: 477964
URI: http://eprints.soton.ac.uk/id/eprint/477964
ISSN: 1040-4651
PURE UUID: ca19e869-813d-42c3-92b1-58d993da1a7c
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Date deposited: 19 Jun 2023 16:30
Last modified: 10 Apr 2024 04:02
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Contributors
Author:
Yuqi He
Author:
Kaixuan Zhang
Author:
Shijuan Li
Author:
Xiang Lu
Author:
Hui Zhao
Author:
Chaonan Guan
Author:
Xu Huang
Author:
Yaliang Shi
Author:
Zhen Kang
Author:
Yu Fan
Author:
Wei Li
Author:
Guangsheng Li
Author:
Ou Long
Author:
Yuanyuan Chen
Author:
Mang Hu
Author:
Jianping Cheng
Author:
Bingliang Xu
Author:
Milen I. Georgiev
Author:
Alisdair R. Fernie
Author:
Meiliang Zhou
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