Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Disruption of the endogenous indole glucosinolate pathway impacts the Arabidopsis thaliana root exudation profile and rhizobacterial community

Journal Article · · Rhizosphere
 [1];  [1];  [2];  [3];  [4];  [5];  [5];  [1]
  1. University of Massachusetts, Boston, MA (United States)
  2. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of Zurich (Switzerland)
  3. University of Maryland, College Park, MD (United States)
  4. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  5. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Root exudates are composed of primary and secondary metabolites known to modulate the rhizosphere microbiota. Glucosinolates are defense compounds present in the Brassicaceae family capable of deterring pathogens, herbivores and biotic stressors in the phyllosphere. In addition, traces of glucosinolates and their hydrolyzed byproducts have been found in the soil, suggesting that these secondary metabolites could play a role in the modulation and establishment of the rhizosphere microbial community associated with this family. Here, we used Arabidopsis thaliana mutant lines, including the cyp79B2cyp79B3 double mutant line with a disruption in the indole glucosinolate pathway and atr1D, which overexpresses ATR1 and increases glucosinolate production. These lines were analyzed using liquid chromatography-tandem mass spectrometry (LC-MS/MS) and 16S rRNA amplicon sequencing to evaluate how genetic modifications to the indole glucosinolate pathway affects the root exudate profile of Arabidopsis thaliana, and, in turn, impacts the rhizosphere microbial community. Metabolic analysis of root exudates from the wild-type Columbia (Col-0), along with the mutant lines, confirmed that alterations to the indole glucosinolate biosynthetic pathway result in shifts in the root exudate profile of the plant. We observed changes in the relative abundance of exuded metabolites. Moreover, 16S rRNA amplicon sequencing results provided evidence that the rhizobacterial communities associated with the plant lines used were directly impacted in diversity and community composition. Here, this work provides further information on the involvement of secondary metabolites and their role in modulating the rhizobacterial community. Root metabolites dictate the presence of different bacterial species, including plant growth-promoting rhizobacteria (PGPR). Our results suggest that genetic alterations in the indole glucosinolate pathway cause disruptions beyond the endogenous levels of the plant, significantly changing the abundance and presence of different metabolites in the root exudates of the plants as well as the microbial rhizosphere community.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth & Environmental Systems Science (EESS); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2557475
Alternate ID(s):
OSTI ID: 2531011
Journal Information:
Rhizosphere, Journal Name: Rhizosphere Vol. 33; ISSN 2452-2198
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (75)

Root morphology and exudate availability are shaped by particle size and chemistry in Brachypodium distachyon journal July 2020
Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores journal January 1988
Root exudates: from plant to rhizosphere and beyond journal July 2019
Formation of Simple Nitriles upon Glucosinolate Hydrolysis Affects Direct and Indirect Defense Against the Specialist Herbivore, Pieris rapae journal September 2008
Jasmonic Acid and Ethylene Signaling Pathways Regulate Glucosinolate Levels in Plants During Rhizobacteria-Induced Systemic Resistance Against a Leaf-Chewing Herbivore journal November 2016
Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems journal June 2008
Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle journal March 2005
Devosia rhizoryzae sp. nov., and Devosia oryziradicis sp. nov., novel plant growth promoting members of the genus Devosia, isolated from the rhizosphere of rice plants journal November 2021
Cruciferous Vegetables, Isothiocyanates, and Prevention of Bladder Cancer journal February 2015
Rhizosphere chemical dialogues: plant–microbe interactions journal December 2009
Rhizosphere microbiome: Functional compensatory assembly for plant fitness journal January 2021
Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH journal November 2019
Synthesis, antibacterial properties and bioinformatics computational analyses of novel 8-hydroxyquinoline derivatives journal October 2019
Dealing with the unknown: Metabolomics and Metabolite Atlases journal September 2010
Regulation of Pathogen-Triggered Tryptophan Metabolism in Arabidopsis thaliana by MYB Transcription Factors and Indole Glucosinolate Conversion Products journal May 2016
How does a plant orchestrate defense in time and space? Using glucosinolates in Arabidopsis as case study journal August 2017
Characterization of recombinant nitrile-specifier proteins (NSPs) of Arabidopsis thaliana: Dependency on Fe(II) ions and the effect of glucosinolate substrate and reaction conditions journal December 2012
Controlled atmosphere preserves quality and phytonutrients in wild rocket (Diplotaxis tenuifolia) journal April 2006
Glyphosate effects on soil rhizosphere-associated bacterial communities journal February 2016
Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication journal March 2016
Myrosinase: gene family evolution and herbivore defense in Brassicaceae journal January 2000
Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots journal June 2009
Rhizosphere microbiome assemblage is affected by plant development journal November 2013
A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence journal September 2015
Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking journal August 2016
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion journal October 2020
Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation journal April 2021
Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis journal May 2004
Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis journal February 2000
Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis journal March 2015
Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome journal May 2019
Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots journal December 2021
A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis journal May 1998
Cytochrome P450 CYP79B2 from Arabidopsis Catalyzes the Conversion of Tryptophan to Indole-3-acetaldoxime, a Precursor of Indole Glucosinolates and Indole-3-acetic Acid journal October 2000
Application of Natural Blends of Phytochemicals Derived from the Root Exudates of Arabidopsis to the Soil Reveal That Phenolic-related Compounds Predominantly Modulate the Soil Microbiome journal January 2013
Nitrile-specifier Proteins Involved in Glucosinolate Hydrolysis in Arabidopsis thaliana journal May 2009
Testing hypotheses about the microbiome using the linear decomposition model (LDM) journal April 2020
Microbial co-operation in the rhizosphere journal May 2005
Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates journal April 2009
Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3 journal December 2002
The Arabidopsis ATR1 Myb Transcription Factor Controls Indolic Glucosinolate Homeostasis journal January 2005
Altered Profile of Secondary Metabolites in the Root Exudates of Arabidopsis ATP-Binding Cassette Transporter Mutants journal December 2007
Metabolic and Transcriptomic Changes Induced in Arabidopsis by the Rhizobacterium Pseudomonas fluorescens SS101 journal October 2012
Genetic Control of Natural Variation in Arabidopsis Glucosinolate Accumulation journal June 2001
Glutathione Transferase U13 Functions in Pathogen-Triggered Glucosinolate Metabolism journal November 2017
The Multifunctional Enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) Converts Cysteine-Indole-3-Acetonitrile to Camalexin in the Indole-3-Acetonitrile Metabolic Network ofArabidopsis thaliana    journal June 2009
CYP83B1, a Cytochrome P450 at the Metabolic Branch Point in Auxin and Indole Glucosinolate Biosynthesis in Arabidopsis journal January 2001
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies journal October 2015
Functional genomics tools to decipher the pathogenicity mechanisms of the necrotrophic fungus Plectosphaerella cucumerina in Arabidopsis thaliana journal September 2012
Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism: Involvement of MTA/SAH nucleosidase in bacterial metabolism journal November 2010
Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses journal June 2004
The myrosinase‐glucosinolate system, its organisation and biochemistry journal May 1996
Causes and consequences of plant-associated biofilms: Causes and consequences of plant-associated biofilms journal May 2008
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass journal January 2019
Plant glucosinolate biosynthesis and breakdown pathways shape the rhizosphere bacterial/archaeal community journal February 2024
In Vitro Activity of Glucosinolates and Their Degradation Products against Brassica-Pathogenic Bacteria and Fungi journal January 2015
Antiseptics and Disinfectants: Activity, Action, and Resistance journal January 1999
Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns journal March 2017
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data journal July 2010
Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin journal May 2018
Enterobacteriaceae dominate the core microbiome and contribute to the resistome of arugula (Eruca sativa Mill.) journal January 2019
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions journal February 2013
Degradation of Biofumigant Isothiocyanates and Allyl Glucosinolate in Soil and Their Effects on the Microbial Community Composition journal July 2015
The ecodist Package for Dissimilarity-based Analysis of Ecological Data journal January 2007
The Split-Apply-Combine Strategy for Data Analysis journal January 2011
Least-Squares Means: The R Package lsmeans journal January 2016
Welcome to the Tidyverse journal November 2019
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton journal June 2015
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases journal July 2015
The Earth Microbiome Project: Meeting report of the “1st EMP meeting on sample selection and acquisition” at Argonne National Laboratory October 6th 2010. journal January 2010
Rhizospheric pseudomonads journal December 2008
Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere journal August 2009
Malioxamycin, a new antibiotic with spheroplast-forming activity. I. Producing organism, fermentation, isolation and characterization. journal January 1980

Similar Records

Indole Glucosinolate Biosynthesis Limits Phenylpropanoid Accumulation in Arabidopsis thaliana
Journal Article · Fri May 01 00:00:00 EDT 2015 · The Plant Cell · OSTI ID:1597755

Glucosinolate and phenylpropanoid biosynthesis are linked by proteasome-dependent degradation of PAL
Journal Article · Tue Aug 13 00:00:00 EDT 2019 · New Phytologist · OSTI ID:1597911