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Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)

Pleurotus eryngii (king oyster mushroom) is a commercially important mushroom with high nutritional and economic value. However, soft rot disease, caused by the pathogenic bacterium Erwinia beijingensis, poses a threat to its quality and production. Morphological and ultrastructural observations of...

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Autores principales: Gao, Qi, Liu, Yu, Xie, Jianbo, Zhao, Shuang, Qin, Wentao, Song, Qinggang, Wang, Shouxian, Rong, Chengbo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241817/
https://www.ncbi.nlm.nih.gov/pubmed/35616396
http://dx.doi.org/10.1128/spectrum.01445-22
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author Gao, Qi
Liu, Yu
Xie, Jianbo
Zhao, Shuang
Qin, Wentao
Song, Qinggang
Wang, Shouxian
Rong, Chengbo
author_facet Gao, Qi
Liu, Yu
Xie, Jianbo
Zhao, Shuang
Qin, Wentao
Song, Qinggang
Wang, Shouxian
Rong, Chengbo
author_sort Gao, Qi
collection PubMed
description Pleurotus eryngii (king oyster mushroom) is a commercially important mushroom with high nutritional and economic value. However, soft rot disease, caused by the pathogenic bacterium Erwinia beijingensis, poses a threat to its quality and production. Morphological and ultrastructural observations of P. eryngii were conducted at early, middle, and late stages of infection. At 2 days postinoculation (dpi), small yellow spots on the fruiting body were observed. The infected tissue displayed hyphal deformations and breaks at 5 dpi. At 9 dpi, damage to cell wall integrity and absence of intact cellular organelles were observed and the diseased fruiting bodies were unable to grow normally. Transcriptome analysis identified 4,296 differentially expressed genes in the fruiting body following infection. In fact, broad transcriptional reprogramming was observed in infected fruiting bodies compared to controls. The affected pathways included antioxidant systems, peroxisome biogenesis, autophagy, and oxidation-reduction. More specifically, pex genes were downregulated during infection, indicating impaired peroxisome homeostasis and redox balance. Additionally, genes encoding chitinase, β-1,3-glucanase, and proteases associated with cell wall degradation were upregulated in infected P. eryngii. This study provides insights into the responses of P. eryngii during soft rot disease and facilitates the understanding of the pathogenic process of bacteriosis in mushrooms. IMPORTANCE Pleurotus eryngii (king oyster mushroom) is a popular and economically valuable edible mushroom; however, it suffers from various bacterial diseases, including soft rot disease caused by the bacterium Erwinia beijingensis. Here, we examined bacterial infection of the mushroom through morphological and ultrastructural observations as well as transcriptome analysis. Pathogen attack damaged the cell structure of P. eryngii, including the cell wall, and also induced high levels of reactive oxygen species. These results were reflected in differential gene expression in P. eryngii as a response to the pathogenic bacteria, including genes involved in antioxidant systems, peroxisome biogenesis, autophagy, oxidation-reduction, ribosome biogenesis, and cell-wall degradation, among others. This study provides insights into the structural and molecular responses of P. eryngii during soft rot disease, improving our understanding and the potential control of the pathogenic process of bacteriosis in mushrooms.
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spelling pubmed-92418172022-06-30 Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii) Gao, Qi Liu, Yu Xie, Jianbo Zhao, Shuang Qin, Wentao Song, Qinggang Wang, Shouxian Rong, Chengbo Microbiol Spectr Research Article Pleurotus eryngii (king oyster mushroom) is a commercially important mushroom with high nutritional and economic value. However, soft rot disease, caused by the pathogenic bacterium Erwinia beijingensis, poses a threat to its quality and production. Morphological and ultrastructural observations of P. eryngii were conducted at early, middle, and late stages of infection. At 2 days postinoculation (dpi), small yellow spots on the fruiting body were observed. The infected tissue displayed hyphal deformations and breaks at 5 dpi. At 9 dpi, damage to cell wall integrity and absence of intact cellular organelles were observed and the diseased fruiting bodies were unable to grow normally. Transcriptome analysis identified 4,296 differentially expressed genes in the fruiting body following infection. In fact, broad transcriptional reprogramming was observed in infected fruiting bodies compared to controls. The affected pathways included antioxidant systems, peroxisome biogenesis, autophagy, and oxidation-reduction. More specifically, pex genes were downregulated during infection, indicating impaired peroxisome homeostasis and redox balance. Additionally, genes encoding chitinase, β-1,3-glucanase, and proteases associated with cell wall degradation were upregulated in infected P. eryngii. This study provides insights into the responses of P. eryngii during soft rot disease and facilitates the understanding of the pathogenic process of bacteriosis in mushrooms. IMPORTANCE Pleurotus eryngii (king oyster mushroom) is a popular and economically valuable edible mushroom; however, it suffers from various bacterial diseases, including soft rot disease caused by the bacterium Erwinia beijingensis. Here, we examined bacterial infection of the mushroom through morphological and ultrastructural observations as well as transcriptome analysis. Pathogen attack damaged the cell structure of P. eryngii, including the cell wall, and also induced high levels of reactive oxygen species. These results were reflected in differential gene expression in P. eryngii as a response to the pathogenic bacteria, including genes involved in antioxidant systems, peroxisome biogenesis, autophagy, oxidation-reduction, ribosome biogenesis, and cell-wall degradation, among others. This study provides insights into the structural and molecular responses of P. eryngii during soft rot disease, improving our understanding and the potential control of the pathogenic process of bacteriosis in mushrooms. American Society for Microbiology 2022-05-26 /pmc/articles/PMC9241817/ /pubmed/35616396 http://dx.doi.org/10.1128/spectrum.01445-22 Text en Copyright © 2022 Gao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Gao, Qi
Liu, Yu
Xie, Jianbo
Zhao, Shuang
Qin, Wentao
Song, Qinggang
Wang, Shouxian
Rong, Chengbo
Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title_full Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title_fullStr Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title_full_unstemmed Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title_short Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii)
title_sort bacterial infection induces ultrastructural and transcriptional changes in the king oyster mushroom (pleurotus eryngii)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241817/
https://www.ncbi.nlm.nih.gov/pubmed/35616396
http://dx.doi.org/10.1128/spectrum.01445-22
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