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Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum

Biological control is a promising approach to suppress diseases caused by Pythium spp. such as Pythium soft rot of ginger caused by P. myriotylum. Unusually for a single genus, it also includes species that can antagonize Pythium plant pathogens, such as Pythium oligandrum. We investigated if a new...

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Autores principales: Daly, Paul, Chen, Siqiao, Xue, Taiqiang, Li, Jingjing, Sheikh, Taha Majid Mahmood, Zhang, Qimeng, Wang, Xuehai, Zhang, Jinfeng, Fitzpatrick, David A., McGowan, Jamie, Shi, Xiujuan, Deng, Sheng, Jiu, Min, Zhou, Dongmei, Druzhinina, Irina S., Wei, Lihui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8637047/
https://www.ncbi.nlm.nih.gov/pubmed/34867897
http://dx.doi.org/10.3389/fmicb.2021.765872
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author Daly, Paul
Chen, Siqiao
Xue, Taiqiang
Li, Jingjing
Sheikh, Taha Majid Mahmood
Zhang, Qimeng
Wang, Xuehai
Zhang, Jinfeng
Fitzpatrick, David A.
McGowan, Jamie
Shi, Xiujuan
Deng, Sheng
Jiu, Min
Zhou, Dongmei
Druzhinina, Irina S.
Wei, Lihui
author_facet Daly, Paul
Chen, Siqiao
Xue, Taiqiang
Li, Jingjing
Sheikh, Taha Majid Mahmood
Zhang, Qimeng
Wang, Xuehai
Zhang, Jinfeng
Fitzpatrick, David A.
McGowan, Jamie
Shi, Xiujuan
Deng, Sheng
Jiu, Min
Zhou, Dongmei
Druzhinina, Irina S.
Wei, Lihui
author_sort Daly, Paul
collection PubMed
description Biological control is a promising approach to suppress diseases caused by Pythium spp. such as Pythium soft rot of ginger caused by P. myriotylum. Unusually for a single genus, it also includes species that can antagonize Pythium plant pathogens, such as Pythium oligandrum. We investigated if a new isolate of P. oligandrum could antagonize P. myriotylum, what changes occurred in gene expression when P. oligandrum (antagonist) and P. myriotylum (host) interacted, and whether P. oligandrum could control soft-rot of ginger caused by P. myriotylum. An isolate of P. oligandrum, GAQ1, recovered from soil could antagonize P. myriotylum in a plate-based confrontation assay whereby P. myriotylum became non-viable. The loss of viability of P. myriotylum coupled with how P. oligandrum hyphae could coil around and penetrate the hyphae of P. myriotylum, indicated a predatory interaction. We investigated the transcriptional responses of P. myriotylum and P. oligandrum using dual-RNAseq at a stage in the confrontation where similar levels of total transcripts were measured from each species. As part of the transcriptional response of P. myriotylum to the presence of P. oligandrum, genes including a subset of putative Kazal-type protease inhibitors were strongly upregulated along with cellulases, elicitin-like proteins and genes involved in the repair of DNA double-strand breaks. In P. oligandrum, proteases, cellulases, and peroxidases featured prominently in the upregulated genes. The upregulation along with constitutive expression of P. oligandrum proteases appeared to be responded to by the upregulation of putative protease inhibitors from P. myriotylum, suggesting a P. myriotylum defensive strategy. Notwithstanding this P. myriotylum defensive strategy, P. oligandrum had a strong disease control effect on soft-rot of ginger caused by P. myriotylum. The newly isolated strain of P. oligandrum is a promising biocontrol agent for suppressing the soft-rot of ginger. The dual-RNAseq approach highlights responses of P. myriotylum that suggests features of a defensive strategy, and are perhaps another factor that may contribute to the variable success and durability of biological attempts to control diseases caused by Pythium spp.
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spelling pubmed-86370472021-12-03 Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum Daly, Paul Chen, Siqiao Xue, Taiqiang Li, Jingjing Sheikh, Taha Majid Mahmood Zhang, Qimeng Wang, Xuehai Zhang, Jinfeng Fitzpatrick, David A. McGowan, Jamie Shi, Xiujuan Deng, Sheng Jiu, Min Zhou, Dongmei Druzhinina, Irina S. Wei, Lihui Front Microbiol Microbiology Biological control is a promising approach to suppress diseases caused by Pythium spp. such as Pythium soft rot of ginger caused by P. myriotylum. Unusually for a single genus, it also includes species that can antagonize Pythium plant pathogens, such as Pythium oligandrum. We investigated if a new isolate of P. oligandrum could antagonize P. myriotylum, what changes occurred in gene expression when P. oligandrum (antagonist) and P. myriotylum (host) interacted, and whether P. oligandrum could control soft-rot of ginger caused by P. myriotylum. An isolate of P. oligandrum, GAQ1, recovered from soil could antagonize P. myriotylum in a plate-based confrontation assay whereby P. myriotylum became non-viable. The loss of viability of P. myriotylum coupled with how P. oligandrum hyphae could coil around and penetrate the hyphae of P. myriotylum, indicated a predatory interaction. We investigated the transcriptional responses of P. myriotylum and P. oligandrum using dual-RNAseq at a stage in the confrontation where similar levels of total transcripts were measured from each species. As part of the transcriptional response of P. myriotylum to the presence of P. oligandrum, genes including a subset of putative Kazal-type protease inhibitors were strongly upregulated along with cellulases, elicitin-like proteins and genes involved in the repair of DNA double-strand breaks. In P. oligandrum, proteases, cellulases, and peroxidases featured prominently in the upregulated genes. The upregulation along with constitutive expression of P. oligandrum proteases appeared to be responded to by the upregulation of putative protease inhibitors from P. myriotylum, suggesting a P. myriotylum defensive strategy. Notwithstanding this P. myriotylum defensive strategy, P. oligandrum had a strong disease control effect on soft-rot of ginger caused by P. myriotylum. The newly isolated strain of P. oligandrum is a promising biocontrol agent for suppressing the soft-rot of ginger. The dual-RNAseq approach highlights responses of P. myriotylum that suggests features of a defensive strategy, and are perhaps another factor that may contribute to the variable success and durability of biological attempts to control diseases caused by Pythium spp. Frontiers Media S.A. 2021-11-16 /pmc/articles/PMC8637047/ /pubmed/34867897 http://dx.doi.org/10.3389/fmicb.2021.765872 Text en Copyright © 2021 Daly, Chen, Xue, Li, Sheikh, Zhang, Wang, Zhang, Fitzpatrick, McGowan, Shi, Deng, Jiu, Zhou, Druzhinina and Wei. 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
Daly, Paul
Chen, Siqiao
Xue, Taiqiang
Li, Jingjing
Sheikh, Taha Majid Mahmood
Zhang, Qimeng
Wang, Xuehai
Zhang, Jinfeng
Fitzpatrick, David A.
McGowan, Jamie
Shi, Xiujuan
Deng, Sheng
Jiu, Min
Zhou, Dongmei
Druzhinina, Irina S.
Wei, Lihui
Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title_full Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title_fullStr Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title_full_unstemmed Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title_short Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum
title_sort dual-transcriptomic, microscopic, and biocontrol analyses of the interaction between the bioeffector pythium oligandrum and the pythium soft-rot of ginger pathogen pythium myriotylum
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8637047/
https://www.ncbi.nlm.nih.gov/pubmed/34867897
http://dx.doi.org/10.3389/fmicb.2021.765872
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