Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai
ABSTRACT Dickeya fangzhongdai is a devastating bacterial pathogen infecting a wide range of crops and ornamental plants worldwide. As a newly identified bacterial species in 2016, the regulatory mechanisms that govern its virulence are still a mystery. In this study, we explored the potential roles...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01965-23 |
| _version_ | 1827586651906375680 |
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| author | Congcong Xie Weihan Gu Zhongqiao Chen Zhibin Liang Shufen Huang Lian-Hui Zhang Shaohua Chen |
| author_facet | Congcong Xie Weihan Gu Zhongqiao Chen Zhibin Liang Shufen Huang Lian-Hui Zhang Shaohua Chen |
| author_sort | Congcong Xie |
| collection | DOAJ |
| description | ABSTRACT Dickeya fangzhongdai is a devastating bacterial pathogen infecting a wide range of crops and ornamental plants worldwide. As a newly identified bacterial species in 2016, the regulatory mechanisms that govern its virulence are still a mystery. In this study, we explored the potential roles of polyamine-mediated cell-to-cell communication in regulation of D. fangzhongdai virulence. Null mutation of speA and speC in D. fangzhongdai strain ZXC1, which encodes polyamine biosynthesis through arginine and ornithine pathways, respectively, dramatically reduced bacterial motility, decreased production of plant cell wall degradation (PCWD) enzymes, and attenuated the bacterial virulence on taro and potato. We then tested the effect of various polyamine molecules in the restoration of the mutant phenotypes and showed that putrescine was the most potent signal in the regulation of virulence traits in strain ZXC1. In addition, we found that taro extract contained active signals to rescue putrescine-deficient phenotypes. High-performance liquid chromatography mass spectrometry analysis validated the speA was essential for production of putrescine in D. fangzhongdai ZXC1. We further showed that the putrescine transporters PotF and PlaP are required for putrescine-mediated cell-to-cell communication and virulence against taro and potato tubers. quantitative reverse transcription-PCR analysis demonstrated that putrescine influences the pathogenicity of D. fangzhongdai ZXC1 by regulating the expression of PCWD enzymes, bacterial chemotaxis, and flagellar-related genes. The findings from this study shed a new light for elucidating the pathogenic mechanisms of D. fangzhongdai and present useful clues for developing relevant disease control strategies. IMPORTANCE Dickeya fangzhongdai is a newly identified plant bacterial pathogen with a wide host range. A clear understanding of the cell-to-cell communication systems that modulate the bacterial virulence is of key importance for elucidating its pathogenic mechanisms and for disease control. In this study, we present evidence that putrescine molecules from the pathogen and host plants play an essential role in regulating the bacterial virulence. The significance of this study is in (i) demonstrating that putrescine signaling system regulates D. fangzhongdai virulence mainly through modulating the bacterial motility and production of PCWD enzymes, (ii) outlining the signaling and regulatory mechanisms with which putrescine signaling system modulates the above virulence traits, and (iii) validating that D. fangzhongdai could use both arginine and ornithine pathways to synthesize putrescine signals. To our knowledge, this is the first report to show that putrescine signaling system plays a key role in modulating the pathogenicity of D. fangzhongdai. |
| first_indexed | 2024-03-09T00:04:44Z |
| format | Article |
| id | doaj.art-1aba038ea014457d8e6aa831b311c65a |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:04:44Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj.art-1aba038ea014457d8e6aa831b311c65a2023-12-12T13:17:21ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.01965-23Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdaiCongcong Xie0Weihan Gu1Zhongqiao Chen2Zhibin Liang3Shufen Huang4Lian-Hui Zhang5Shaohua Chen6National Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaNational Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University Integrative Microbiology Research Centre , Guangzhou, ChinaABSTRACT Dickeya fangzhongdai is a devastating bacterial pathogen infecting a wide range of crops and ornamental plants worldwide. As a newly identified bacterial species in 2016, the regulatory mechanisms that govern its virulence are still a mystery. In this study, we explored the potential roles of polyamine-mediated cell-to-cell communication in regulation of D. fangzhongdai virulence. Null mutation of speA and speC in D. fangzhongdai strain ZXC1, which encodes polyamine biosynthesis through arginine and ornithine pathways, respectively, dramatically reduced bacterial motility, decreased production of plant cell wall degradation (PCWD) enzymes, and attenuated the bacterial virulence on taro and potato. We then tested the effect of various polyamine molecules in the restoration of the mutant phenotypes and showed that putrescine was the most potent signal in the regulation of virulence traits in strain ZXC1. In addition, we found that taro extract contained active signals to rescue putrescine-deficient phenotypes. High-performance liquid chromatography mass spectrometry analysis validated the speA was essential for production of putrescine in D. fangzhongdai ZXC1. We further showed that the putrescine transporters PotF and PlaP are required for putrescine-mediated cell-to-cell communication and virulence against taro and potato tubers. quantitative reverse transcription-PCR analysis demonstrated that putrescine influences the pathogenicity of D. fangzhongdai ZXC1 by regulating the expression of PCWD enzymes, bacterial chemotaxis, and flagellar-related genes. The findings from this study shed a new light for elucidating the pathogenic mechanisms of D. fangzhongdai and present useful clues for developing relevant disease control strategies. IMPORTANCE Dickeya fangzhongdai is a newly identified plant bacterial pathogen with a wide host range. A clear understanding of the cell-to-cell communication systems that modulate the bacterial virulence is of key importance for elucidating its pathogenic mechanisms and for disease control. In this study, we present evidence that putrescine molecules from the pathogen and host plants play an essential role in regulating the bacterial virulence. The significance of this study is in (i) demonstrating that putrescine signaling system regulates D. fangzhongdai virulence mainly through modulating the bacterial motility and production of PCWD enzymes, (ii) outlining the signaling and regulatory mechanisms with which putrescine signaling system modulates the above virulence traits, and (iii) validating that D. fangzhongdai could use both arginine and ornithine pathways to synthesize putrescine signals. To our knowledge, this is the first report to show that putrescine signaling system plays a key role in modulating the pathogenicity of D. fangzhongdai.https://journals.asm.org/doi/10.1128/spectrum.01965-23Dickeya fangzhongdaipolyaminesbacterial motilityplant cell wall-degrading enzymespathogenicity |
| spellingShingle | Congcong Xie Weihan Gu Zhongqiao Chen Zhibin Liang Shufen Huang Lian-Hui Zhang Shaohua Chen Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai Microbiology Spectrum Dickeya fangzhongdai polyamines bacterial motility plant cell wall-degrading enzymes pathogenicity |
| title | Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai |
| title_full | Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai |
| title_fullStr | Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai |
| title_full_unstemmed | Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai |
| title_short | Polyamine signaling communications play a key role in regulating the pathogenicity of Dickeya fangzhongdai |
| title_sort | polyamine signaling communications play a key role in regulating the pathogenicity of dickeya fangzhongdai |
| topic | Dickeya fangzhongdai polyamines bacterial motility plant cell wall-degrading enzymes pathogenicity |
| url | https://journals.asm.org/doi/10.1128/spectrum.01965-23 |
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