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Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions

Soybean Sclerotinia stem rot is caused by Sclerotinia sclerotiorum infection, which causes extensive and severe damage to soybean production. Here, we isolated and patented a Bacillus amyloliquefaciens strain, and used it to verify the antagonistic effect of B. amyloliquefaciens on S. sclerotiorum a...

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Autores principales: Cheng, Yunqing, Gao, Xin, He, Hongli, Zhang, Xingzheng, Wang, Ran, Liu, Jianfeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9260588/
https://www.ncbi.nlm.nih.gov/pubmed/35814672
http://dx.doi.org/10.3389/fmicb.2022.924313
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author Cheng, Yunqing
Gao, Xin
He, Hongli
Zhang, Xingzheng
Wang, Ran
Liu, Jianfeng
author_facet Cheng, Yunqing
Gao, Xin
He, Hongli
Zhang, Xingzheng
Wang, Ran
Liu, Jianfeng
author_sort Cheng, Yunqing
collection PubMed
description Soybean Sclerotinia stem rot is caused by Sclerotinia sclerotiorum infection, which causes extensive and severe damage to soybean production. Here, we isolated and patented a Bacillus amyloliquefaciens strain, and used it to verify the antagonistic effect of B. amyloliquefaciens on S. sclerotiorum and to explore the possible underlying mechanism. First, we conducted a plate confrontation experiment using the two microbes. Then, inoculation of soybean (Glycine max) seedlings with S. sclerotiorum (Gm-Ss), B. amyloliquefaciens (Gm-Ba), and their combination (Gm-Ba-Ss) was performed, followed by dual RNA sequencing analysis. Plate confrontation and inoculation experiments showed that B. amyloliquefaciens significantly antagonized S. sclerotiorum growth. The average number of fragments per kilobase of transcript per million fragments mapped of S. sclerotiorum transcripts in Gm-Ss and Gm-Ba-Ss inoculation treatments were 117.82 and 50.79, respectively, indicating that B. amyloliquefaciens strongly inhibited gene expression of S. sclerotiorum. In contrast, the average number of fragments per kilobase of transcript per million fragments mapped of B. amyloliquefaciens transcripts in Gm-Ba and Gm-Ba-Ss inoculation treatments were 479.56 and 579.66, respectively, indicating that S. sclerotiorum promoted overall gene expression in B. amyloliquefaciens. For S. sclerotiorum, 507 upregulated and 4,950 downregulated genes were identified among 8,975 genes in the paired comparison Gm-Ba-Ss vs. Gm-Ss. These differentially expressed genes (DEGs) were significantly enriched in the ribosome (ko03010) KEGG pathway. Additionally, for B. amyloliquefaciens, 294 upregulated and 178 downregulated genes were identified among all 3,154 genes in the paired comparison Gm-Ba-Ss vs. Gm-Ba, and these DEGs were mainly and significantly enriched in metabolism-related KEGG pathways, including the citrate cycle (ko00020) and carbon metabolism (ko01200). We concluded that B. amyloliquefaciens inhibits the expression of genes encoding the ribosomal subunit of S. sclerotiorum, resulting in protein synthesis inhibition in S. sclerotiorum, and thus had a strong antagonistic effect on the fungus. This study provides a scientific basis for the biological control of S. sclerotiorum by B. amyloliquefaciens.
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spelling pubmed-92605882022-07-08 Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions Cheng, Yunqing Gao, Xin He, Hongli Zhang, Xingzheng Wang, Ran Liu, Jianfeng Front Microbiol Microbiology Soybean Sclerotinia stem rot is caused by Sclerotinia sclerotiorum infection, which causes extensive and severe damage to soybean production. Here, we isolated and patented a Bacillus amyloliquefaciens strain, and used it to verify the antagonistic effect of B. amyloliquefaciens on S. sclerotiorum and to explore the possible underlying mechanism. First, we conducted a plate confrontation experiment using the two microbes. Then, inoculation of soybean (Glycine max) seedlings with S. sclerotiorum (Gm-Ss), B. amyloliquefaciens (Gm-Ba), and their combination (Gm-Ba-Ss) was performed, followed by dual RNA sequencing analysis. Plate confrontation and inoculation experiments showed that B. amyloliquefaciens significantly antagonized S. sclerotiorum growth. The average number of fragments per kilobase of transcript per million fragments mapped of S. sclerotiorum transcripts in Gm-Ss and Gm-Ba-Ss inoculation treatments were 117.82 and 50.79, respectively, indicating that B. amyloliquefaciens strongly inhibited gene expression of S. sclerotiorum. In contrast, the average number of fragments per kilobase of transcript per million fragments mapped of B. amyloliquefaciens transcripts in Gm-Ba and Gm-Ba-Ss inoculation treatments were 479.56 and 579.66, respectively, indicating that S. sclerotiorum promoted overall gene expression in B. amyloliquefaciens. For S. sclerotiorum, 507 upregulated and 4,950 downregulated genes were identified among 8,975 genes in the paired comparison Gm-Ba-Ss vs. Gm-Ss. These differentially expressed genes (DEGs) were significantly enriched in the ribosome (ko03010) KEGG pathway. Additionally, for B. amyloliquefaciens, 294 upregulated and 178 downregulated genes were identified among all 3,154 genes in the paired comparison Gm-Ba-Ss vs. Gm-Ba, and these DEGs were mainly and significantly enriched in metabolism-related KEGG pathways, including the citrate cycle (ko00020) and carbon metabolism (ko01200). We concluded that B. amyloliquefaciens inhibits the expression of genes encoding the ribosomal subunit of S. sclerotiorum, resulting in protein synthesis inhibition in S. sclerotiorum, and thus had a strong antagonistic effect on the fungus. This study provides a scientific basis for the biological control of S. sclerotiorum by B. amyloliquefaciens. Frontiers Media S.A. 2022-06-23 /pmc/articles/PMC9260588/ /pubmed/35814672 http://dx.doi.org/10.3389/fmicb.2022.924313 Text en Copyright © 2022 Cheng, Gao, He, Zhang, Wang and Liu. 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 Microbiology
Cheng, Yunqing
Gao, Xin
He, Hongli
Zhang, Xingzheng
Wang, Ran
Liu, Jianfeng
Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title_full Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title_fullStr Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title_full_unstemmed Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title_short Dual RNA Sequencing Analysis of Bacillus amyloliquefaciens and Sclerotinia sclerotiorum During Infection of Soybean Seedlings by S. sclerotiorum Unveils Antagonistic Interactions
title_sort dual rna sequencing analysis of bacillus amyloliquefaciens and sclerotinia sclerotiorum during infection of soybean seedlings by s. sclerotiorum unveils antagonistic interactions
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9260588/
https://www.ncbi.nlm.nih.gov/pubmed/35814672
http://dx.doi.org/10.3389/fmicb.2022.924313
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