Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions

ABSTRACT Iron (Fe) availability has well-known effects on plant and microbial metabolism, but its effects on interspecies interactions are poorly understood. The purpose of this study was to investigate metabolite exchange between the grass Brachypodium distachyon strain Bd21 and the soil bacterium...

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Autores principales:	Rene M. Boiteau, Lye Meng Markillie, David W. Hoyt, Dehong Hu, Rosalie K. Chu, Hugh D. Mitchell, Ljiljana Pasa-Tolic, Janet K. Jansson, Christer Jansson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	iron grass siderophore Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4741e9b20cb645a8ab3f1c6cd0f102fa
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spelling	oai:doaj.org-article:4741e9b20cb645a8ab3f1c6cd0f102fa2021-12-02T19:22:16ZMetabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions10.1128/mSystems.00580-202379-5077https://doaj.org/article/4741e9b20cb645a8ab3f1c6cd0f102fa2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00580-20https://doaj.org/toc/2379-5077ABSTRACT Iron (Fe) availability has well-known effects on plant and microbial metabolism, but its effects on interspecies interactions are poorly understood. The purpose of this study was to investigate metabolite exchange between the grass Brachypodium distachyon strain Bd21 and the soil bacterium Pseudomonas fluorescens SBW25::gfp/lux (SBW25) during Fe limitation under axenic conditions. We compared the transcriptional profiles and root exudate metabolites of B. distachyon plants grown semihydroponically with and without SBW25 inoculation and Fe amendment. Liquid chromatography-mass spectrometry analysis of the hydroponic solution revealed an increase in the abundance of the phytosiderophores mugineic acid and deoxymugineic acid under Fe-limited conditions compared to Fe-replete conditions, indicating greater secretion by roots presumably to facilitate Fe uptake. In SBW25-inoculated roots, expression of genes encoding phytosiderophore biosynthesis and uptake proteins increased compared to that in sterile roots, but external phytosiderophore abundances decreased. P. fluorescens siderophores were not detected in treatments without Fe. Rather, expression of SBW25 genes encoding a porin, a transporter, and a monooxygenase was significantly upregulated in response to Fe deprivation. Collectively, these results suggest that SBW25 consumed root-exuded phytosiderophores in response to Fe deficiency, and we propose target genes that may be involved. SBW25 also altered the expression of root genes encoding defense-related enzymes and regulators, including thionin and cyanogenic glycoside production, chitinase, and peroxidase activity, and transcription factors. Our findings provide insights into the molecular bases for the stress response and metabolite exchange of interacting plants and bacteria under Fe-deficient conditions. IMPORTANCE Rhizosphere bacteria influence the growth of their host plant by consuming and producing metabolites, nutrients, and antibiotic compounds within the root system that affect plant metabolism. Under Fe-limited growth conditions, different plant and microbial species have distinct Fe acquisition strategies, often involving the secretion of strong Fe-binding chelators that scavenge Fe and facilitate uptake. Here, we studied interactions between P. fluorescens SBW25, a plant-colonizing bacterium that produces siderophores with antifungal properties, and B. distachyon, a genetic model for cereal grain and biofuel grasses. Under controlled growth conditions, bacterial siderophore production was inhibited in the root system of Fe-deficient plants, bacterial inoculation altered transcription of genes involved in defense and stress response in the roots of B. distachyon, and SBW25 degraded phytosiderophores secreted by the host plant. These findings provide mechanistic insight into interactions that may play a role in rhizosphere dynamics and plant health in soils with low Fe solubility.Rene M. BoiteauLye Meng MarkillieDavid W. HoytDehong HuRosalie K. ChuHugh D. MitchellLjiljana Pasa-TolicJanet K. JanssonChrister JanssonAmerican Society for MicrobiologyarticleirongrasssiderophoreMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	iron grass siderophore Microbiology QR1-502
spellingShingle	iron grass siderophore Microbiology QR1-502 Rene M. Boiteau Lye Meng Markillie David W. Hoyt Dehong Hu Rosalie K. Chu Hugh D. Mitchell Ljiljana Pasa-Tolic Janet K. Jansson Christer Jansson Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
description	ABSTRACT Iron (Fe) availability has well-known effects on plant and microbial metabolism, but its effects on interspecies interactions are poorly understood. The purpose of this study was to investigate metabolite exchange between the grass Brachypodium distachyon strain Bd21 and the soil bacterium Pseudomonas fluorescens SBW25::gfp/lux (SBW25) during Fe limitation under axenic conditions. We compared the transcriptional profiles and root exudate metabolites of B. distachyon plants grown semihydroponically with and without SBW25 inoculation and Fe amendment. Liquid chromatography-mass spectrometry analysis of the hydroponic solution revealed an increase in the abundance of the phytosiderophores mugineic acid and deoxymugineic acid under Fe-limited conditions compared to Fe-replete conditions, indicating greater secretion by roots presumably to facilitate Fe uptake. In SBW25-inoculated roots, expression of genes encoding phytosiderophore biosynthesis and uptake proteins increased compared to that in sterile roots, but external phytosiderophore abundances decreased. P. fluorescens siderophores were not detected in treatments without Fe. Rather, expression of SBW25 genes encoding a porin, a transporter, and a monooxygenase was significantly upregulated in response to Fe deprivation. Collectively, these results suggest that SBW25 consumed root-exuded phytosiderophores in response to Fe deficiency, and we propose target genes that may be involved. SBW25 also altered the expression of root genes encoding defense-related enzymes and regulators, including thionin and cyanogenic glycoside production, chitinase, and peroxidase activity, and transcription factors. Our findings provide insights into the molecular bases for the stress response and metabolite exchange of interacting plants and bacteria under Fe-deficient conditions. IMPORTANCE Rhizosphere bacteria influence the growth of their host plant by consuming and producing metabolites, nutrients, and antibiotic compounds within the root system that affect plant metabolism. Under Fe-limited growth conditions, different plant and microbial species have distinct Fe acquisition strategies, often involving the secretion of strong Fe-binding chelators that scavenge Fe and facilitate uptake. Here, we studied interactions between P. fluorescens SBW25, a plant-colonizing bacterium that produces siderophores with antifungal properties, and B. distachyon, a genetic model for cereal grain and biofuel grasses. Under controlled growth conditions, bacterial siderophore production was inhibited in the root system of Fe-deficient plants, bacterial inoculation altered transcription of genes involved in defense and stress response in the roots of B. distachyon, and SBW25 degraded phytosiderophores secreted by the host plant. These findings provide mechanistic insight into interactions that may play a role in rhizosphere dynamics and plant health in soils with low Fe solubility.
format	article
author	Rene M. Boiteau Lye Meng Markillie David W. Hoyt Dehong Hu Rosalie K. Chu Hugh D. Mitchell Ljiljana Pasa-Tolic Janet K. Jansson Christer Jansson
author_facet	Rene M. Boiteau Lye Meng Markillie David W. Hoyt Dehong Hu Rosalie K. Chu Hugh D. Mitchell Ljiljana Pasa-Tolic Janet K. Jansson Christer Jansson
author_sort	Rene M. Boiteau
title	Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
title_short	Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
title_full	Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
title_fullStr	Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
title_full_unstemmed	Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions
title_sort	metabolic interactions between <italic toggle="yes">brachypodium</italic> and <named-content content-type="genus-species">pseudomonas fluorescens</named-content> under controlled iron-limited conditions
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/4741e9b20cb645a8ab3f1c6cd0f102fa
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Metabolic Interactions between <italic toggle="yes">Brachypodium</italic> and <named-content content-type="genus-species">Pseudomonas fluorescens</named-content> under Controlled Iron-Limited Conditions

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