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Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota
Plants and animals are in constant association with a variety of microbes. Although much is known about how pathogenic and symbiotic microbes interact with plants, less is known about the population dynamics, adaptive traits, and transcriptional features of the vast number of microbes that make up t...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9168490/ https://www.ncbi.nlm.nih.gov/pubmed/35344425 http://dx.doi.org/10.1073/pnas.2114460119 |
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author | Velásquez, André C. Huguet-Tapia, José C. He, Sheng Yang |
author_facet | Velásquez, André C. Huguet-Tapia, José C. He, Sheng Yang |
author_sort | Velásquez, André C. |
collection | PubMed |
description | Plants and animals are in constant association with a variety of microbes. Although much is known about how pathogenic and symbiotic microbes interact with plants, less is known about the population dynamics, adaptive traits, and transcriptional features of the vast number of microbes that make up the bulk of the plant microbiota. The majority of microbiota taxa are either commensal, natural mutants of pathogens, or pathogens that encounter strong immune responses due to plant recognition of pathogen effectors. How these “nonpathogenic” microbes interact with plants is poorly understood, especially during long-term, steady-state interactions, which are more reflective of plant–microbiota interactions in nature. In this study, we embarked upon long-term population and in planta transcriptomic studies of commensal endophytic bacteria and compared them to nonpathogenic or effector-triggered immunity-inducing strains of the bacterial pathogen Pseudomonas syringae. Our results led to the discovery of multiplication–death equilibrium as a common basis for the shared long-term static population densities of these bacteria. A comprehensive in planta transcriptomic analysis using multiple time points after inoculation revealed a striking similarity between the transcriptomic features of nonpathogenic P. syringae to that of bacteria in stationary phase in vitro, a metabolically active physiological state in which the production of adaptive secondary metabolites and stress responses are induced. We propose that the long-term population and transcriptomic features of nonpathogenic bacteria captured in this study likely reflect the physiological steady state encountered by the bulk of endophytic microbiota—excluding virulent pathogens—in their life-long interactions with plants in nature. |
format | Online Article Text |
id | pubmed-9168490 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-91684902022-06-07 Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota Velásquez, André C. Huguet-Tapia, José C. He, Sheng Yang Proc Natl Acad Sci U S A Biological Sciences Plants and animals are in constant association with a variety of microbes. Although much is known about how pathogenic and symbiotic microbes interact with plants, less is known about the population dynamics, adaptive traits, and transcriptional features of the vast number of microbes that make up the bulk of the plant microbiota. The majority of microbiota taxa are either commensal, natural mutants of pathogens, or pathogens that encounter strong immune responses due to plant recognition of pathogen effectors. How these “nonpathogenic” microbes interact with plants is poorly understood, especially during long-term, steady-state interactions, which are more reflective of plant–microbiota interactions in nature. In this study, we embarked upon long-term population and in planta transcriptomic studies of commensal endophytic bacteria and compared them to nonpathogenic or effector-triggered immunity-inducing strains of the bacterial pathogen Pseudomonas syringae. Our results led to the discovery of multiplication–death equilibrium as a common basis for the shared long-term static population densities of these bacteria. A comprehensive in planta transcriptomic analysis using multiple time points after inoculation revealed a striking similarity between the transcriptomic features of nonpathogenic P. syringae to that of bacteria in stationary phase in vitro, a metabolically active physiological state in which the production of adaptive secondary metabolites and stress responses are induced. We propose that the long-term population and transcriptomic features of nonpathogenic bacteria captured in this study likely reflect the physiological steady state encountered by the bulk of endophytic microbiota—excluding virulent pathogens—in their life-long interactions with plants in nature. National Academy of Sciences 2022-03-28 2022-04-05 /pmc/articles/PMC9168490/ /pubmed/35344425 http://dx.doi.org/10.1073/pnas.2114460119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Velásquez, André C. Huguet-Tapia, José C. He, Sheng Yang Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title | Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title_full | Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title_fullStr | Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title_full_unstemmed | Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title_short | Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
title_sort | shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9168490/ https://www.ncbi.nlm.nih.gov/pubmed/35344425 http://dx.doi.org/10.1073/pnas.2114460119 |
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