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Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea
Botrytis cinerea, the causal agent of gray mold, is an important plant pathogen causing preharvest and postharvest diseases. Due to the extensive use of commercial fungicides, fungicide-resistant strains have emerged. Natural compounds with antifungal properties are widely present in various kinds o...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269628/ https://www.ncbi.nlm.nih.gov/pubmed/37191530 http://dx.doi.org/10.1128/spectrum.00526-23 |
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author | Wang, Guanbo Wang, Yadi Wang, Kunchun Zhao, Haonan Liu, Mengjie Liang, Wenxing Li, Delong |
author_facet | Wang, Guanbo Wang, Yadi Wang, Kunchun Zhao, Haonan Liu, Mengjie Liang, Wenxing Li, Delong |
author_sort | Wang, Guanbo |
collection | PubMed |
description | Botrytis cinerea, the causal agent of gray mold, is an important plant pathogen causing preharvest and postharvest diseases. Due to the extensive use of commercial fungicides, fungicide-resistant strains have emerged. Natural compounds with antifungal properties are widely present in various kinds of organisms. Perillaldehyde (PA), derived from the plant species Perilla frutescens, is generally recognized as a potent antimicrobial substance and to be safe to humans and the environment. In this study, we demonstrated that PA could significantly inhibit the mycelial growth of B. cinerea and reduced its pathogenicity on tomato leaves. We also found that PA had a significant protective effect on tomato, grape, and strawberry. The antifungal mechanism of PA was investigated by measuring the reactive oxygen species (ROS) accumulation, the intracellular Ca(2+) level, the mitochondrial membrane potential, DNA fragmentation, and phosphatidylserine exposure. Further analyses revealed that PA promoted protein ubiquitination and induced autophagic activities and then triggered protein degradation. When the two metacaspase genes, BcMca1 and BcMca2, were knocked out from B. cinerea, all mutants did not exhibit reduced sensitivity to PA. These findings demonstrated that PA could induce metacaspase-independent apoptosis in B. cinerea. Based on our results, we proposed that PA could be used as an effective control agent for gray mold management. IMPORTANCE Botrytis cinerea causes gray mold disease, is considered one of the most important dangerous pathogens worldwide, and leads to severe economic losses worldwide. Due to the lack of resistant varieties of B. cinerea, gray mold control has mainly relied on application of synthetic fungicides. However, long-term and extensive use of synthetic fungicides has increased fungicide resistance in B. cinerea and is harmful to humans and the environment. In this study, we found that perillaldehyde has a significant protective effect on tomato, grape, and strawberry. We further characterized the antifungal mechanism of PA on B. cinerea. Our results indicated that PA induced apoptosis that was independent of metacaspase function. |
format | Online Article Text |
id | pubmed-10269628 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-102696282023-06-16 Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea Wang, Guanbo Wang, Yadi Wang, Kunchun Zhao, Haonan Liu, Mengjie Liang, Wenxing Li, Delong Microbiol Spectr Research Article Botrytis cinerea, the causal agent of gray mold, is an important plant pathogen causing preharvest and postharvest diseases. Due to the extensive use of commercial fungicides, fungicide-resistant strains have emerged. Natural compounds with antifungal properties are widely present in various kinds of organisms. Perillaldehyde (PA), derived from the plant species Perilla frutescens, is generally recognized as a potent antimicrobial substance and to be safe to humans and the environment. In this study, we demonstrated that PA could significantly inhibit the mycelial growth of B. cinerea and reduced its pathogenicity on tomato leaves. We also found that PA had a significant protective effect on tomato, grape, and strawberry. The antifungal mechanism of PA was investigated by measuring the reactive oxygen species (ROS) accumulation, the intracellular Ca(2+) level, the mitochondrial membrane potential, DNA fragmentation, and phosphatidylserine exposure. Further analyses revealed that PA promoted protein ubiquitination and induced autophagic activities and then triggered protein degradation. When the two metacaspase genes, BcMca1 and BcMca2, were knocked out from B. cinerea, all mutants did not exhibit reduced sensitivity to PA. These findings demonstrated that PA could induce metacaspase-independent apoptosis in B. cinerea. Based on our results, we proposed that PA could be used as an effective control agent for gray mold management. IMPORTANCE Botrytis cinerea causes gray mold disease, is considered one of the most important dangerous pathogens worldwide, and leads to severe economic losses worldwide. Due to the lack of resistant varieties of B. cinerea, gray mold control has mainly relied on application of synthetic fungicides. However, long-term and extensive use of synthetic fungicides has increased fungicide resistance in B. cinerea and is harmful to humans and the environment. In this study, we found that perillaldehyde has a significant protective effect on tomato, grape, and strawberry. We further characterized the antifungal mechanism of PA on B. cinerea. Our results indicated that PA induced apoptosis that was independent of metacaspase function. American Society for Microbiology 2023-05-16 /pmc/articles/PMC10269628/ /pubmed/37191530 http://dx.doi.org/10.1128/spectrum.00526-23 Text en Copyright © 2023 Wang 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 Wang, Guanbo Wang, Yadi Wang, Kunchun Zhao, Haonan Liu, Mengjie Liang, Wenxing Li, Delong Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title | Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title_full | Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title_fullStr | Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title_full_unstemmed | Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title_short | Perillaldehyde Functions as a Potential Antifungal Agent by Triggering Metacaspase-Independent Apoptosis in Botrytis cinerea |
title_sort | perillaldehyde functions as a potential antifungal agent by triggering metacaspase-independent apoptosis in botrytis cinerea |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269628/ https://www.ncbi.nlm.nih.gov/pubmed/37191530 http://dx.doi.org/10.1128/spectrum.00526-23 |
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