Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew

Powdery mildew is a fungal disease devastating to wheat, causing significant quality and yield loss. Flavonoids are important secondary plant metabolites that confer resistance to biotic and abiotic stress. However, whether they play a role in powdery mildew resistance in wheat has yet to be explore...

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Main Authors: Wenjing Xu, Xiaoyi Xu, Ran Han, Xiaolu Wang, Kai Wang, Guang Qi, Pengtao Ma, Takao Komatsuda, Cheng Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1125194/full
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author Wenjing Xu
Wenjing Xu
Wenjing Xu
Wenjing Xu
Xiaoyi Xu
Ran Han
Ran Han
Ran Han
Ran Han
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Kai Wang
Kai Wang
Kai Wang
Kai Wang
Guang Qi
Guang Qi
Guang Qi
Guang Qi
Pengtao Ma
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Cheng Liu
Cheng Liu
Cheng Liu
Cheng Liu
author_facet Wenjing Xu
Wenjing Xu
Wenjing Xu
Wenjing Xu
Xiaoyi Xu
Ran Han
Ran Han
Ran Han
Ran Han
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Kai Wang
Kai Wang
Kai Wang
Kai Wang
Guang Qi
Guang Qi
Guang Qi
Guang Qi
Pengtao Ma
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Cheng Liu
Cheng Liu
Cheng Liu
Cheng Liu
author_sort Wenjing Xu
collection DOAJ
description Powdery mildew is a fungal disease devastating to wheat, causing significant quality and yield loss. Flavonoids are important secondary plant metabolites that confer resistance to biotic and abiotic stress. However, whether they play a role in powdery mildew resistance in wheat has yet to be explored. In the present study, we combined transcriptome and metabolome analyses to compare differentially expressed genes (DEGs) and differentially accumulated flavonoids identified in plants with and without powdery mildew inoculation. Transcriptome analysis identified 4,329 DEGs in susceptible wheat cv. Jimai229, and 8,493 in resistant cv. HHG46. The DEGs were functionally enriched using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes, revealing the flavonoid synthesis pathway as the most significant in both cultivars. This was consistent with the upregulation of flavonoid synthesis pathway genes observed by quantitative PCR. Metabolome analysis indicated flavone and flavonol biosynthesis pathways as the most significantly enriched following powdery mildew inoculation. An accumulation of total flavonoids content was also found to be induced by powdery mildew infection. Exogenous flavonoids treatment of inoculated plants led to less severe infection, with fewer and smaller powdery mildew spots on the wheat leaves. This reduction is speculated to be regulated through malondialdehyde content and the activities of peroxidase and catalase. Our study provides a fundamental theory for further exploration of the potential of flavonoids as biological prevention and control agents against powdery mildew in wheat.
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spelling doaj.art-f127729be11f47928452a61d560081872023-02-01T07:03:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-02-011410.3389/fpls.2023.11251941125194Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildewWenjing Xu0Wenjing Xu1Wenjing Xu2Wenjing Xu3Xiaoyi Xu4Ran Han5Ran Han6Ran Han7Ran Han8Xiaolu Wang9Xiaolu Wang10Xiaolu Wang11Xiaolu Wang12Kai Wang13Kai Wang14Kai Wang15Kai Wang16Guang Qi17Guang Qi18Guang Qi19Guang Qi20Pengtao Ma21Takao Komatsuda22Takao Komatsuda23Takao Komatsuda24Takao Komatsuda25Cheng Liu26Cheng Liu27Cheng Liu28Cheng Liu29Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaSchool of Life Sciences, Yantai University, Yantai, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaSchool of Life Sciences, Yantai University, Yantai, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, ChinaNational Engineering Laboratory of Wheat and Maize, Jinan, Shandong, ChinaKey Laboratory of Wheat Biology and Genetic Improvement in the North Huang and Huai River Valley of Ministry of Agriculture, Jinan, Shandong, ChinaShandong Wheat Technology Innovation Center, Jinan, Shandong, ChinaPowdery mildew is a fungal disease devastating to wheat, causing significant quality and yield loss. Flavonoids are important secondary plant metabolites that confer resistance to biotic and abiotic stress. However, whether they play a role in powdery mildew resistance in wheat has yet to be explored. In the present study, we combined transcriptome and metabolome analyses to compare differentially expressed genes (DEGs) and differentially accumulated flavonoids identified in plants with and without powdery mildew inoculation. Transcriptome analysis identified 4,329 DEGs in susceptible wheat cv. Jimai229, and 8,493 in resistant cv. HHG46. The DEGs were functionally enriched using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes, revealing the flavonoid synthesis pathway as the most significant in both cultivars. This was consistent with the upregulation of flavonoid synthesis pathway genes observed by quantitative PCR. Metabolome analysis indicated flavone and flavonol biosynthesis pathways as the most significantly enriched following powdery mildew inoculation. An accumulation of total flavonoids content was also found to be induced by powdery mildew infection. Exogenous flavonoids treatment of inoculated plants led to less severe infection, with fewer and smaller powdery mildew spots on the wheat leaves. This reduction is speculated to be regulated through malondialdehyde content and the activities of peroxidase and catalase. Our study provides a fundamental theory for further exploration of the potential of flavonoids as biological prevention and control agents against powdery mildew in wheat.https://www.frontiersin.org/articles/10.3389/fpls.2023.1125194/fullwheatpowdery mildewtranscriptomemetabolomeflavonoids
spellingShingle Wenjing Xu
Wenjing Xu
Wenjing Xu
Wenjing Xu
Xiaoyi Xu
Ran Han
Ran Han
Ran Han
Ran Han
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Xiaolu Wang
Kai Wang
Kai Wang
Kai Wang
Kai Wang
Guang Qi
Guang Qi
Guang Qi
Guang Qi
Pengtao Ma
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Takao Komatsuda
Cheng Liu
Cheng Liu
Cheng Liu
Cheng Liu
Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
Frontiers in Plant Science
wheat
powdery mildew
transcriptome
metabolome
flavonoids
title Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
title_full Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
title_fullStr Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
title_full_unstemmed Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
title_short Integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
title_sort integrated transcriptome and metabolome analysis reveals that flavonoids function in wheat resistance to powdery mildew
topic wheat
powdery mildew
transcriptome
metabolome
flavonoids
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1125194/full
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