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Title: Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings

Abstract

Plants, fungi, and bacteria form complex, mutually-beneficial communities within the soil environment. In return for photosynthetically derived sugars in the form of exudates from plant roots, the microbial symbionts in these rhizosphere communities provide their host plants access to otherwise inaccessible nutrients in soils and help defend the plant against biotic and abiotic stresses. One role that bacteria may play in these communities is that of Mycorrhizal Helper Bacteria (MHB). MHB are bacteria that facilitate the interactions between plant roots and symbiotic mycorrhizal fungi and, while the effects of MHB on the formation of plant-fungal symbiosis and on plant health have been well documented, the specific molecular mechanisms by which MHB drive gene regulation in plant roots leading to these benefits remain largely uncharacterized. Here, we investigate the effects of the bacterium Pseudomonas fluorescens SBW25 (SBW25) on aspen root transcriptome using a tripartite laboratory community comprised of Populus tremuloides (aspen) seedlings and the ectomycorrhizal fungus Laccaria bicolor (Laccaria). We show that SBW25 has MHB activity and promotes mycorrhization of aspen roots by Laccaria. Using transcriptomic analysis of aspen roots under multiple community compositions, we identify clusters of co-regulated genes associated with mycorrhization, the presence of SBW25, and MHB-associated functions, andmore » we generate a combinatorial logic network that links causal relationships in observed patterns of gene expression in aspen seedling roots in a single Boolean circuit diagram. The predicted regulatory circuit is used to infer regulatory mechanisms associated with MHB activity. In our laboratory conditions, SBW25 increases the ability of Laccaria to form ectomycorrhizal interactions with aspen seedling roots through the suppression of aspen root antifungal defense responses. Analysis of transcriptomic data identifies that potential molecular mechanisms in aspen roots that respond to MHB activity are proteins with homology to pollen recognition sensors. Pollen recognition sensors integrate multiple environmental signals to down-regulate pollenization-associated gene clusters, making proteins with homology to this system an excellent fit for a predicted mechanism that integrates information from the rhizosphere to down-regulate antifungal defense response genes in the root. These results provide a deeper understanding of aspen gene regulation in response to MHB and suggest additional, hypothesis-driven biological experiments to validate putative molecular mechanisms of MHB activity in the aspen-Laccaria ectomycorrhizal symbiosis.« less

Authors:
; ; ; ; ;
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618605
Alternate Identifier(s):
OSTI ID: 1510073
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Published Article
Journal Name:
BMC Plant Biology
Additional Journal Information:
Journal Name: BMC Plant Biology Journal Volume: 19 Journal Issue: 1; Journal ID: ISSN 1471-2229
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Ectomycorrhiza; Laccaria bicolor; Populus tremuloides; Receptors; transcriptomics

Citation Formats

Shinde, Shalaka, Zerbs, Sarah, Collart, Frank R., Cumming, Jonathan R., Noirot, Philippe, and Larsen, Peter E. Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings. United Kingdom: N. p., 2019. Web. doi:10.1186/s12870-018-1610-0.
Shinde, Shalaka, Zerbs, Sarah, Collart, Frank R., Cumming, Jonathan R., Noirot, Philippe, & Larsen, Peter E. Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings. United Kingdom. https://doi.org/10.1186/s12870-018-1610-0
Shinde, Shalaka, Zerbs, Sarah, Collart, Frank R., Cumming, Jonathan R., Noirot, Philippe, and Larsen, Peter E. Thu . "Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings". United Kingdom. https://doi.org/10.1186/s12870-018-1610-0.
@article{osti_1618605,
title = {Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings},
author = {Shinde, Shalaka and Zerbs, Sarah and Collart, Frank R. and Cumming, Jonathan R. and Noirot, Philippe and Larsen, Peter E.},
abstractNote = {Plants, fungi, and bacteria form complex, mutually-beneficial communities within the soil environment. In return for photosynthetically derived sugars in the form of exudates from plant roots, the microbial symbionts in these rhizosphere communities provide their host plants access to otherwise inaccessible nutrients in soils and help defend the plant against biotic and abiotic stresses. One role that bacteria may play in these communities is that of Mycorrhizal Helper Bacteria (MHB). MHB are bacteria that facilitate the interactions between plant roots and symbiotic mycorrhizal fungi and, while the effects of MHB on the formation of plant-fungal symbiosis and on plant health have been well documented, the specific molecular mechanisms by which MHB drive gene regulation in plant roots leading to these benefits remain largely uncharacterized. Here, we investigate the effects of the bacterium Pseudomonas fluorescens SBW25 (SBW25) on aspen root transcriptome using a tripartite laboratory community comprised of Populus tremuloides (aspen) seedlings and the ectomycorrhizal fungus Laccaria bicolor (Laccaria). We show that SBW25 has MHB activity and promotes mycorrhization of aspen roots by Laccaria. Using transcriptomic analysis of aspen roots under multiple community compositions, we identify clusters of co-regulated genes associated with mycorrhization, the presence of SBW25, and MHB-associated functions, and we generate a combinatorial logic network that links causal relationships in observed patterns of gene expression in aspen seedling roots in a single Boolean circuit diagram. The predicted regulatory circuit is used to infer regulatory mechanisms associated with MHB activity. In our laboratory conditions, SBW25 increases the ability of Laccaria to form ectomycorrhizal interactions with aspen seedling roots through the suppression of aspen root antifungal defense responses. Analysis of transcriptomic data identifies that potential molecular mechanisms in aspen roots that respond to MHB activity are proteins with homology to pollen recognition sensors. Pollen recognition sensors integrate multiple environmental signals to down-regulate pollenization-associated gene clusters, making proteins with homology to this system an excellent fit for a predicted mechanism that integrates information from the rhizosphere to down-regulate antifungal defense response genes in the root. These results provide a deeper understanding of aspen gene regulation in response to MHB and suggest additional, hypothesis-driven biological experiments to validate putative molecular mechanisms of MHB activity in the aspen-Laccaria ectomycorrhizal symbiosis.},
doi = {10.1186/s12870-018-1610-0},
journal = {BMC Plant Biology},
number = 1,
volume = 19,
place = {United Kingdom},
year = {Thu Jan 03 00:00:00 EST 2019},
month = {Thu Jan 03 00:00:00 EST 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s12870-018-1610-0

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Cited by: 19 works
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