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Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere

Plants and their associated microbiota share ecological and evolutionary traits that are considered to be inseparably woven. Their coexistence foresees the use of similar metabolic pathways, leading to the generation of molecules that can cross-regulate each other’s metabolism and ultimately influen...

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Autores principales: Carril, Pablo, Cruz, Joana, di Serio, Claudia, Pieraccini, Giuseppe, Ait Bessai, Sylia, Tenreiro, Rogério, Cruz, Cristina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8733462/
https://www.ncbi.nlm.nih.gov/pubmed/35003023
http://dx.doi.org/10.3389/fmicb.2021.792921
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author Carril, Pablo
Cruz, Joana
di Serio, Claudia
Pieraccini, Giuseppe
Ait Bessai, Sylia
Tenreiro, Rogério
Cruz, Cristina
author_facet Carril, Pablo
Cruz, Joana
di Serio, Claudia
Pieraccini, Giuseppe
Ait Bessai, Sylia
Tenreiro, Rogério
Cruz, Cristina
author_sort Carril, Pablo
collection PubMed
description Plants and their associated microbiota share ecological and evolutionary traits that are considered to be inseparably woven. Their coexistence foresees the use of similar metabolic pathways, leading to the generation of molecules that can cross-regulate each other’s metabolism and ultimately influence plant phenotype. However, the extent to which the microbiota contributes to the overall plant metabolic landscape remains largely unexplored. Due to their early presence in the seed, seed-borne endophytic bacteria can intimately colonize the plant’s endosphere while conferring a series of phytobeneficial services to their host. Understanding the dynamics of these endophytic communities is a crucial step toward the formulation of microbial inoculants that can modulate the functionality of the plant-associated microbiota for improved plant fitness. In this work, wheat (Triticum aestivum) roots non-inoculated and inoculated with the bacterium Herbaspirillum seropedicae strain RAM10 were analyzed to explore the impact of inoculant–endophyte–wheat interrelationships on the regulation of tryptophan (Trp) metabolism in the endosphere environment. Root inoculation with H. seropedicae led to phylum-specific changes in the cultivable seed-borne endophytic community. This modulation shifted the metabolic potential of the community in light of its capacity to modulate the levels of key Trp-related metabolites involved in both indole-3-acetic acid (IAA) biosynthesis and in the kynurenine pathway. Our results support a mode of action of H. seropedicae relying on a shift in both the composition and functionality of the seed-borne endophytic community, which may govern important processes such as root growth. We finally provide a conceptual framework illustrating that interactions among roots, inoculants, and seed-borne endophytes are critical to fine-tuning the levels of IAA in the endosphere. Understanding the outcomes of these interactions is a crucial step toward the formulation of microbial inoculants based on their joint action with seed-borne endophytic communities to promote crop growth and health in a sustainable manner.
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spelling pubmed-87334622022-01-07 Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere Carril, Pablo Cruz, Joana di Serio, Claudia Pieraccini, Giuseppe Ait Bessai, Sylia Tenreiro, Rogério Cruz, Cristina Front Microbiol Microbiology Plants and their associated microbiota share ecological and evolutionary traits that are considered to be inseparably woven. Their coexistence foresees the use of similar metabolic pathways, leading to the generation of molecules that can cross-regulate each other’s metabolism and ultimately influence plant phenotype. However, the extent to which the microbiota contributes to the overall plant metabolic landscape remains largely unexplored. Due to their early presence in the seed, seed-borne endophytic bacteria can intimately colonize the plant’s endosphere while conferring a series of phytobeneficial services to their host. Understanding the dynamics of these endophytic communities is a crucial step toward the formulation of microbial inoculants that can modulate the functionality of the plant-associated microbiota for improved plant fitness. In this work, wheat (Triticum aestivum) roots non-inoculated and inoculated with the bacterium Herbaspirillum seropedicae strain RAM10 were analyzed to explore the impact of inoculant–endophyte–wheat interrelationships on the regulation of tryptophan (Trp) metabolism in the endosphere environment. Root inoculation with H. seropedicae led to phylum-specific changes in the cultivable seed-borne endophytic community. This modulation shifted the metabolic potential of the community in light of its capacity to modulate the levels of key Trp-related metabolites involved in both indole-3-acetic acid (IAA) biosynthesis and in the kynurenine pathway. Our results support a mode of action of H. seropedicae relying on a shift in both the composition and functionality of the seed-borne endophytic community, which may govern important processes such as root growth. We finally provide a conceptual framework illustrating that interactions among roots, inoculants, and seed-borne endophytes are critical to fine-tuning the levels of IAA in the endosphere. Understanding the outcomes of these interactions is a crucial step toward the formulation of microbial inoculants based on their joint action with seed-borne endophytic communities to promote crop growth and health in a sustainable manner. Frontiers Media S.A. 2021-12-23 /pmc/articles/PMC8733462/ /pubmed/35003023 http://dx.doi.org/10.3389/fmicb.2021.792921 Text en Copyright © 2021 Carril, Cruz, di Serio, Pieraccini, Ait Bessai, Tenreiro and Cruz. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Carril, Pablo
Cruz, Joana
di Serio, Claudia
Pieraccini, Giuseppe
Ait Bessai, Sylia
Tenreiro, Rogério
Cruz, Cristina
Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title_full Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title_fullStr Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title_full_unstemmed Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title_short Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere
title_sort modulation of the wheat seed-borne bacterial community by herbaspirillum seropedicae ram10 and its potential effects for tryptophan metabolism in the root endosphere
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8733462/
https://www.ncbi.nlm.nih.gov/pubmed/35003023
http://dx.doi.org/10.3389/fmicb.2021.792921
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