Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato

Abstract Background APETALA2/ethylene responsive factor (AP2/ERF) transcription factors are a plant-specific family of transcription factors and one of the largest families of transcription factors. Ethylene response factors (ERF) regulate plant growth, development, and responses to biotic and abiot...

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Main Authors: Huanhuan Yang, Yaoguang Sun, Hexuan Wang, Tingting Zhao, Xiangyang Xu, Jingbin Jiang, Jingfu Li
Format: Article
Language:English
Published: BMC 2021-02-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-021-02848-3
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author Huanhuan Yang
Yaoguang Sun
Hexuan Wang
Tingting Zhao
Xiangyang Xu
Jingbin Jiang
Jingfu Li
author_facet Huanhuan Yang
Yaoguang Sun
Hexuan Wang
Tingting Zhao
Xiangyang Xu
Jingbin Jiang
Jingfu Li
author_sort Huanhuan Yang
collection DOAJ
description Abstract Background APETALA2/ethylene responsive factor (AP2/ERF) transcription factors are a plant-specific family of transcription factors and one of the largest families of transcription factors. Ethylene response factors (ERF) regulate plant growth, development, and responses to biotic and abiotic stress. In a previous study, the ERF2 gene was significantly upregulated in both resistant and susceptible tomato cultivars in response to Stemphylium lycopersici. The main purpose of this study was to systematically analyze the ERF family and to explore the mechanism of ERF2 in tomato plants resisting pathogen infection by the Virus-induced Gene Silencing technique. Results In this experiment, 134 ERF genes were explored and subjected to bioinformatic analysis and divided into twelve groups. The spatiotemporal expression characteristics of ERF transcription factor gene family in tomato were diverse. Combined with RNA-seq, we found that the expression of 18 ERF transcription factors increased after inoculation with S. lycopersici. In ERF2-silenced plants, the susceptible phenotype was observed after inoculation with S. lycopersici. The hypersensitive response and ROS production were decreased in the ERF2-silenced plants. Physiological analyses showed that the superoxide dismutase, peroxidase and catalase activities were lower in ERF2-silenced plants than in control plants, and the SA and JA contents were lower in ERF2-silenced plants than in control plants after inoculation with S. lycopersici. Furthermore, the results indicated that ERF2 may directly or indirectly regulate Pto, PR1b1 and PR-P2 expression and enhance tomato resistance. Conclusions In this study, we identified and analyzed members of the tomato ERF family by bioinformatics methods and classified, described and analyzed these genes. Subsequently, we used VIGS technology to significantly reduce the expression of ERF2 in tomatoes. The results showed that ERF2 had a positive effect on tomato resistance to S. lycopersici. Interestingly, ERF2 played a key role in multiple SA, JA and ROS signaling pathways to confer resistance to invasion by S. lycopersici. In addition, ERF2 may directly or indirectly regulate Pto, PR1b1 and PR-P2 expression and enhance tomato resistance to S. lycopersici. In summary, this study provides gene resources for breeding for disease resistance in tomato.
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spelling doaj.art-49b4c6172dfe4e2dac6b7397591489ba2022-12-21T22:46:23ZengBMCBMC Plant Biology1471-22292021-02-0121111310.1186/s12870-021-02848-3Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomatoHuanhuan Yang0Yaoguang Sun1Hexuan Wang2Tingting Zhao3Xiangyang Xu4Jingbin Jiang5Jingfu Li6Laboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityLaboratory of Genetic Breeding in Tomato, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture and Landscape Architecture, Northeast Agricultural UniversityAbstract Background APETALA2/ethylene responsive factor (AP2/ERF) transcription factors are a plant-specific family of transcription factors and one of the largest families of transcription factors. Ethylene response factors (ERF) regulate plant growth, development, and responses to biotic and abiotic stress. In a previous study, the ERF2 gene was significantly upregulated in both resistant and susceptible tomato cultivars in response to Stemphylium lycopersici. The main purpose of this study was to systematically analyze the ERF family and to explore the mechanism of ERF2 in tomato plants resisting pathogen infection by the Virus-induced Gene Silencing technique. Results In this experiment, 134 ERF genes were explored and subjected to bioinformatic analysis and divided into twelve groups. The spatiotemporal expression characteristics of ERF transcription factor gene family in tomato were diverse. Combined with RNA-seq, we found that the expression of 18 ERF transcription factors increased after inoculation with S. lycopersici. In ERF2-silenced plants, the susceptible phenotype was observed after inoculation with S. lycopersici. The hypersensitive response and ROS production were decreased in the ERF2-silenced plants. Physiological analyses showed that the superoxide dismutase, peroxidase and catalase activities were lower in ERF2-silenced plants than in control plants, and the SA and JA contents were lower in ERF2-silenced plants than in control plants after inoculation with S. lycopersici. Furthermore, the results indicated that ERF2 may directly or indirectly regulate Pto, PR1b1 and PR-P2 expression and enhance tomato resistance. Conclusions In this study, we identified and analyzed members of the tomato ERF family by bioinformatics methods and classified, described and analyzed these genes. Subsequently, we used VIGS technology to significantly reduce the expression of ERF2 in tomatoes. The results showed that ERF2 had a positive effect on tomato resistance to S. lycopersici. Interestingly, ERF2 played a key role in multiple SA, JA and ROS signaling pathways to confer resistance to invasion by S. lycopersici. In addition, ERF2 may directly or indirectly regulate Pto, PR1b1 and PR-P2 expression and enhance tomato resistance to S. lycopersici. In summary, this study provides gene resources for breeding for disease resistance in tomato.https://doi.org/10.1186/s12870-021-02848-3TomatoEthylene response factors, ERF2Disease resistanceS. Lycopersici
spellingShingle Huanhuan Yang
Yaoguang Sun
Hexuan Wang
Tingting Zhao
Xiangyang Xu
Jingbin Jiang
Jingfu Li
Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
BMC Plant Biology
Tomato
Ethylene response factors, ERF2
Disease resistance
S. Lycopersici
title Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
title_full Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
title_fullStr Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
title_full_unstemmed Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
title_short Genome-wide identification and functional analysis of the ERF2 gene family in response to disease resistance against Stemphylium lycopersici in tomato
title_sort genome wide identification and functional analysis of the erf2 gene family in response to disease resistance against stemphylium lycopersici in tomato
topic Tomato
Ethylene response factors, ERF2
Disease resistance
S. Lycopersici
url https://doi.org/10.1186/s12870-021-02848-3
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