Title: Metabolic Interactions between Brachypodium and Pseudomonas fluorescens under Controlled Iron-Limited Conditions

Abstract

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 genesmore » 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.« less

Authors:

Boiteau, Rene M. ;

• Search DOE PAGES for author "Boiteau, Rene M."
• Search DOE PAGES for ORCID "0000-0002-4127-4417"

Markillie, Lye Meng; Hoyt, David W. ;

• Search DOE PAGES for author "Hoyt, David W."
• Search DOE PAGES for ORCID "0000-0002-2857-719X"

Hu, Dehong ;

• Search DOE PAGES for author "Hu, Dehong"
• Search DOE PAGES for ORCID "0000-0002-3974-2963"

Chu, Rosalie K.; Mitchell, Hugh D.; Pasa-Tolic, Ljiljana ;

• Search DOE PAGES for author "Pasa-Tolic, Ljiljana"
• Search DOE PAGES for ORCID "0000-0001-9853-5457"

Jansson, Janet K.; Jansson, Christer; Bulgarelli, ed., Davide

Publication Date:

Tue Jan 05 00:00:00 EST 2021

Research Org.:

Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1755462

Alternate Identifier(s):

OSTI ID: 1765540

Report Number(s):

PNNL-SA-159673
Journal ID: ISSN 2379-5077; e00580-20

Grant/Contract Number:  

AC05-76RL01830

Resource Type:

Published Article

Journal Name:

mSystems

Additional Journal Information:

Journal Name: mSystems Journal Volume: 6 Journal Issue: 1; Journal ID: ISSN 2379-5077

Publisher:

American Society for Microbiology

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES