Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage

Clubroot disease caused by the obligate parasite <i>Plasmodiophora brassicae</i> is a serious threat to cabbage production worldwide. Current clubroot control primarily relies on a fungicide, but this has a negative impact on the environment and the use of a single biocontrol agent canno...

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Main Authors: Lanfang Wei, Jun Yang, Waqar Ahmed, Xinying Xiong, Qi Liu, Qiong Huang, Guanghai Ji
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Agronomy
Subjects:
Online Access:https://www.mdpi.com/2073-4395/11/12/2424
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author Lanfang Wei
Jun Yang
Waqar Ahmed
Xinying Xiong
Qi Liu
Qiong Huang
Guanghai Ji
author_facet Lanfang Wei
Jun Yang
Waqar Ahmed
Xinying Xiong
Qi Liu
Qiong Huang
Guanghai Ji
author_sort Lanfang Wei
collection DOAJ
description Clubroot disease caused by the obligate parasite <i>Plasmodiophora brassicae</i> is a serious threat to cabbage production worldwide. Current clubroot control primarily relies on a fungicide, but this has a negative impact on the environment and the use of a single biocontrol agent cannot efficiently control the disease. Thus, the combined application of different biocontrol agents has been proposed as a promising alternative. In this study, we used bacterial biocontrol agents as a co-culture (inter-genus and intra-genus) and mono-culture to mitigate the clubroot disease of Chinese cabbage. We evaluated their biocontrol effect and plant growth promoter (PGP) traits in in vitro and in vivo experiments. This study revealed that the inter-genus bacterial co-culture significantly suppresses the incidence of clubroot disease and enhances plant growth compared with intra-genus and mono-culture. In pairwise interaction, we observed that <i>Bacillus cereus</i> BT-23 promotes the growth of <i>Lysobacter antibioticus</i> 13-6 (inter-genus bacterial co-culture), whereas <i>L. capsici</i> ZST1-2 and <i>L. antibioticus</i> 13-6 (intra-genus microbial co-culture) are antagonists to each other. Furthermore, a total of 5575 metabolites, 732 differentially expressed metabolites (DEMs), and 510 unique metabolites were detected through the LC-MS/MS technique in the bacterial co-culture. The number of unique metabolites in inter-genus bacterial co-culture (393 metabolites) was significantly higher than in the intra-genus bacterial co-culture (117 metabolites). Further analysis of DEMs showed that the DEMs were mainly involved in four kinds of metabolism pathways, i.e., carbohydrate metabolism, amino metabolism, nucleotide metabolism, and metabolism of cofactors and vitamins. The contents of some secondary metabolites with biocontrol activity and plant growth-promoting functions were increased in inter-genus bacterial co-culture, indicating that inter-genus bacterial co-culture has a solid potential to suppress clubroot disease. We conclude that the inter-genus bacterial interaction changes the community metabolism and improves several secondary metabolites functions with respect to disease control and PGP ability.
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spelling doaj.art-4fde7e6bd8184a1b8694c64334e7a30f2023-11-23T03:21:40ZengMDPI AGAgronomy2073-43952021-11-011112242410.3390/agronomy11122424Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese CabbageLanfang Wei0Jun Yang1Waqar Ahmed2Xinying Xiong3Qi Liu4Qiong Huang5Guanghai Ji6Key Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaKey Laboratory of Agriculture Biodiversity for Plant Disease Management under the Ministry of Education, Yunnan Agricultural University, Kunming 650201, ChinaClubroot disease caused by the obligate parasite <i>Plasmodiophora brassicae</i> is a serious threat to cabbage production worldwide. Current clubroot control primarily relies on a fungicide, but this has a negative impact on the environment and the use of a single biocontrol agent cannot efficiently control the disease. Thus, the combined application of different biocontrol agents has been proposed as a promising alternative. In this study, we used bacterial biocontrol agents as a co-culture (inter-genus and intra-genus) and mono-culture to mitigate the clubroot disease of Chinese cabbage. We evaluated their biocontrol effect and plant growth promoter (PGP) traits in in vitro and in vivo experiments. This study revealed that the inter-genus bacterial co-culture significantly suppresses the incidence of clubroot disease and enhances plant growth compared with intra-genus and mono-culture. In pairwise interaction, we observed that <i>Bacillus cereus</i> BT-23 promotes the growth of <i>Lysobacter antibioticus</i> 13-6 (inter-genus bacterial co-culture), whereas <i>L. capsici</i> ZST1-2 and <i>L. antibioticus</i> 13-6 (intra-genus microbial co-culture) are antagonists to each other. Furthermore, a total of 5575 metabolites, 732 differentially expressed metabolites (DEMs), and 510 unique metabolites were detected through the LC-MS/MS technique in the bacterial co-culture. The number of unique metabolites in inter-genus bacterial co-culture (393 metabolites) was significantly higher than in the intra-genus bacterial co-culture (117 metabolites). Further analysis of DEMs showed that the DEMs were mainly involved in four kinds of metabolism pathways, i.e., carbohydrate metabolism, amino metabolism, nucleotide metabolism, and metabolism of cofactors and vitamins. The contents of some secondary metabolites with biocontrol activity and plant growth-promoting functions were increased in inter-genus bacterial co-culture, indicating that inter-genus bacterial co-culture has a solid potential to suppress clubroot disease. We conclude that the inter-genus bacterial interaction changes the community metabolism and improves several secondary metabolites functions with respect to disease control and PGP ability.https://www.mdpi.com/2073-4395/11/12/2424<i>Plasmodiophora brassicae</i>biological controldisease incidencebacterial co-culturemetabolomics analysis
spellingShingle Lanfang Wei
Jun Yang
Waqar Ahmed
Xinying Xiong
Qi Liu
Qiong Huang
Guanghai Ji
Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
Agronomy
<i>Plasmodiophora brassicae</i>
biological control
disease incidence
bacterial co-culture
metabolomics analysis
title Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
title_full Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
title_fullStr Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
title_full_unstemmed Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
title_short Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
title_sort unraveling the association between metabolic changes in inter genus and intra genus bacteria to mitigate clubroot disease of chinese cabbage
topic <i>Plasmodiophora brassicae</i>
biological control
disease incidence
bacterial co-culture
metabolomics analysis
url https://www.mdpi.com/2073-4395/11/12/2424
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