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Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean

Soybean Sclerotinia stem rot caused by Sclerotinia sclerotiorum is a common disease in soybean, and effective biological control is urgently needed. We have previously confirmed that Bacillus amyloliquefaciens can effectively antagonize S. sclerotiorum in a plate competition experiment and a soybean...

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Autores principales: Liu, Jianfeng, Hu, Xianwen, He, Hongli, Zhang, Xingzheng, Guo, Jinhua, Bai, Jing, Cheng, Yunqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9666723/
https://www.ncbi.nlm.nih.gov/pubmed/36406417
http://dx.doi.org/10.3389/fmicb.2022.1025771
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author Liu, Jianfeng
Hu, Xianwen
He, Hongli
Zhang, Xingzheng
Guo, Jinhua
Bai, Jing
Cheng, Yunqing
author_facet Liu, Jianfeng
Hu, Xianwen
He, Hongli
Zhang, Xingzheng
Guo, Jinhua
Bai, Jing
Cheng, Yunqing
author_sort Liu, Jianfeng
collection PubMed
description Soybean Sclerotinia stem rot caused by Sclerotinia sclerotiorum is a common disease in soybean, and effective biological control is urgently needed. We have previously confirmed that Bacillus amyloliquefaciens can effectively antagonize S. sclerotiorum in a plate competition experiment and a soybean seedling inoculation experiment. In this study, the mechanisms underlying plant death caused by S. sclerotiorum and soybean resistance to S. sclerotiorum induced by B. amyloliquefaciens were evaluated. The stems of potted soybean seedlings were inoculated with S. sclerotiorum (Gm-Ss), B. amyloliquefaciens (Gm-Ba), and their combination (Gm-Ba-Ss), using scratch treatments as a control, followed by dual RNA sequencing and bioinformatics analyses. Global gene expression levels in the Gm-Ss treatment were much lower than those in the Gm-Ba, Gm-Ba-Ss, and Gm groups, suggesting that S. sclerotiorum strongly inhibited global gene expression in soybean. In a pairwise comparison of Gm-Ss vs. Gm, 19983 differentially expressed genes (DEGs) were identified. Down-regulated DEGs were involved in various KEGG pathways, including ko01110 (biosynthesis of secondary metabolites), ko01100 (metabolic pathways), ko01120 (microbial metabolism in diverse environments), ko00500 (starch and sucrose metabolism), and ko04075 (plant hormone signal transmission), suggesting that S. sclerotiorum inoculation had a serious negative effect on soybean metabolism. In Gm-Ba vs. Gm, 13091 DEGs were identified, and these DEGs were significantly enriched in ko03010 (ribosome) and ko03008 (ribosome biogenesis in eucaryotes). Our results suggest that B. amyloliquefaciens increases the expression of genes encoding the ribosomal subunit, promotes cell wall biogenesis, and induces systemic resistance. S. sclerotiorum strongly inhibited metabolism in soybean, inhibited the synthesis of the cytoskeleton, and induced the up-regulation of programmed death and senescence-related genes via an ethylene signal transduction pathway. These results improve our understanding of S. sclerotiorum-induced plant death and soybean resistance to S. sclerotiorum induced by B. amyloliquefaciens and may contribute to the improvement of strategies to avoid yield losses.
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spelling pubmed-96667232022-11-17 Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean Liu, Jianfeng Hu, Xianwen He, Hongli Zhang, Xingzheng Guo, Jinhua Bai, Jing Cheng, Yunqing Front Microbiol Microbiology Soybean Sclerotinia stem rot caused by Sclerotinia sclerotiorum is a common disease in soybean, and effective biological control is urgently needed. We have previously confirmed that Bacillus amyloliquefaciens can effectively antagonize S. sclerotiorum in a plate competition experiment and a soybean seedling inoculation experiment. In this study, the mechanisms underlying plant death caused by S. sclerotiorum and soybean resistance to S. sclerotiorum induced by B. amyloliquefaciens were evaluated. The stems of potted soybean seedlings were inoculated with S. sclerotiorum (Gm-Ss), B. amyloliquefaciens (Gm-Ba), and their combination (Gm-Ba-Ss), using scratch treatments as a control, followed by dual RNA sequencing and bioinformatics analyses. Global gene expression levels in the Gm-Ss treatment were much lower than those in the Gm-Ba, Gm-Ba-Ss, and Gm groups, suggesting that S. sclerotiorum strongly inhibited global gene expression in soybean. In a pairwise comparison of Gm-Ss vs. Gm, 19983 differentially expressed genes (DEGs) were identified. Down-regulated DEGs were involved in various KEGG pathways, including ko01110 (biosynthesis of secondary metabolites), ko01100 (metabolic pathways), ko01120 (microbial metabolism in diverse environments), ko00500 (starch and sucrose metabolism), and ko04075 (plant hormone signal transmission), suggesting that S. sclerotiorum inoculation had a serious negative effect on soybean metabolism. In Gm-Ba vs. Gm, 13091 DEGs were identified, and these DEGs were significantly enriched in ko03010 (ribosome) and ko03008 (ribosome biogenesis in eucaryotes). Our results suggest that B. amyloliquefaciens increases the expression of genes encoding the ribosomal subunit, promotes cell wall biogenesis, and induces systemic resistance. S. sclerotiorum strongly inhibited metabolism in soybean, inhibited the synthesis of the cytoskeleton, and induced the up-regulation of programmed death and senescence-related genes via an ethylene signal transduction pathway. These results improve our understanding of S. sclerotiorum-induced plant death and soybean resistance to S. sclerotiorum induced by B. amyloliquefaciens and may contribute to the improvement of strategies to avoid yield losses. Frontiers Media S.A. 2022-11-02 /pmc/articles/PMC9666723/ /pubmed/36406417 http://dx.doi.org/10.3389/fmicb.2022.1025771 Text en Copyright © 2022 Liu, Hu, He, Zhang, Guo, Bai and Cheng. 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
Liu, Jianfeng
Hu, Xianwen
He, Hongli
Zhang, Xingzheng
Guo, Jinhua
Bai, Jing
Cheng, Yunqing
Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title_full Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title_fullStr Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title_full_unstemmed Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title_short Digital gene expression profiling of the transcriptional response to Sclerotinia sclerotiorum and its antagonistic bacterium Bacillus amyloliquefaciens in soybean
title_sort digital gene expression profiling of the transcriptional response to sclerotinia sclerotiorum and its antagonistic bacterium bacillus amyloliquefaciens in soybean
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9666723/
https://www.ncbi.nlm.nih.gov/pubmed/36406417
http://dx.doi.org/10.3389/fmicb.2022.1025771
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