skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Genome-wide identification of bacterial plant colonization genes

Journal Article · · PLoS Biology (Online)
ORCiD logo [1];  [2];  [1];  [3];  [2];  [1];  [1];  [4];  [2];  [5];  [1];  [3];  [2];  [6]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Univ. of North Carolina, Chapel Hill, NC (United States). Howard Hughes Medical Inst., Dept. of Biology, Dept. of Microbiology and Immunology
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States). School of Natural Sciences
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Univ. of California, Merced, CA (United States). School of Natural Sciences

Diverse soil-resident bacteria can contribute to plant growth and health, but the molecular mechanisms enabling them to effectively colonize their plant hosts remain poorly understood. We used randomly barcoded transposon mutagenesis sequencing (RB-TnSeq) in Pseudomonas simiae, a model root-colonizing bacterium, to establish a genome-wide map of bacterial genes required for colonization of the Arabidopsis thaliana root system. We identified 115 genes (2% of all P. simiae genes) with functions that are required for maximal competitive colonization of the root system. Among the genes we identified were some with obvious colonization-related roles in motility and carbon metabolism, as well as 44 other genes that had no or vague functional predictions. Independent validation assays of individual genes confirmed colonization functions for 20 of 22 (91%) cases tested. To further characterize genes identified by our screen, we compared the functional contributions of P. simiae genes to growth in 90 distinct in vitro conditions by RB-TnSeq, highlighting specific metabolic functions associated with root colonization genes. Here, our analysis of bacterial genes by sequence-driven saturation mutagenesis revealed a genome-wide map of the genetic determinants of plant root colonization and offers a starting point for targeted improvement of the colonization capabilities of plant-beneficial microbes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF); Gordon and Betty Moore Foundation (GBMF)
Grant/Contract Number:
AC02-05CH11231; F32-GM112345-02; SC0014395; IOS-1343020; GBMF3030
OSTI ID:
1416925
Journal Information:
PLoS Biology (Online), Vol. 15, Issue 9; ISSN 1545-7885
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 102 works
Citation information provided by
Web of Science

References (40)

Microbial life in the phyllosphere journal November 2012
Crystal Structure and Mechanism of the Escherichia coli ArnA (PmrI) Transformylase Domain. An Enzyme for Lipid A Modification with 4-Amino-4-deoxy- l -arabinose and Polymyxin Resistance , journal April 2005
Biological control of soil-borne pathogens by fluorescent pseudomonads journal March 2005
Expanded microbial genome coverage and improved protein family annotation in the COG database journal November 2014
Precision-engineering the Pseudomonas aeruginosa genome with two-step allelic exchange journal October 2015
Exercising influence: distinct biotic interactions shape root microbiomes journal August 2015
Identifying microbial fitness determinants by insertion sequencing using genome-wide transposon mutant libraries journal November 2011
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa journal July 2015
Role of the O-Antigen of Lipopolysaccharide, and Possible Roles of Growth Rate and of NADH:ubiquinone Oxidoreductase ( nuo ) in Competitive Tomato Root-Tip Colonization by Pseudomonas fluorescens WCS365 journal August 1998
DEG 10, an update of the database of essential genes that includes both protein-coding genes and noncoding genomic elements: Table 1. journal November 2013
Innate Immune Responses Activated in Arabidopsis Roots by Microbe-Associated Molecular Patterns journal March 2010
Salicylic Acid, a Multifaceted Hormone to Combat Disease journal September 2009
Roots Shaping Their Microbiome: Global Hotspots for Microbial Activity journal August 2015
Induced Systemic Resistance by Beneficial Microbes journal August 2014
Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417 journal July 2015
Evolution of Plant Pathogenesis in Pseudomonas syringae : A Genomics Perspective journal September 2011
M OLECULAR D ETERMINANTS OF R HIZOSPHERE C OLONIZATION BY P SEUDOMONAS journal September 2001
Functional overlap of the Arabidopsis leaf and root microbiota journal December 2015
Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism journal September 2011
Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons journal May 2015
The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity: Regulation of cAMP by a chemosensory system journal March 2010
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota journal August 2012
Defining the core Arabidopsis thaliana root microbiome journal August 2012
IMG: the integrated microbial genomes database and comparative analysis system journal December 2011
Profiling of secondary metabolites in root exudates of Arabidopsis thaliana journal December 2014
Regulation of Lipid A Modifications by Salmonella typhimurium Virulence Genes phoP-phoQ journal April 1997
The two-component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane: Two-component colR/S system of Pseudomonas fluorescens WCS365 journal November 2006
Unraveling Root Developmental Programs Initiated by Beneficial Pseudomonas spp. Bacteria journal March 2013
Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms journal September 2009
Inside the root microbiome: Bacterial root endophytes and plant growth promotion journal September 2013
The plant immune system journal November 2006
Structure and Functions of the Bacterial Microbiota of Plants journal April 2013
Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. journal August 1996
The Pseudomonas aeruginosa Chp Chemosensory System Regulates Intracellular cAMP Levels by Modulating Adenylate Cyclase Activity text January 2010
Defining the core Arabidopsis thaliana root microbiome text January 2012
Microbial life in the phyllosphere text January 2012
Systemic Resistance in Arabidopsis Induced by Biocontrol Bacteria Is Independent of Salicylic Acid Accumulation and Pathogenesis-Related Gene Expression journal August 1996
Rhizosphere Selection of Highly Motile Phenotypic Variants of Pseudomonas fluorescens with Enhanced Competitive Colonization Ability journal May 2006
Role of the Type III Secreted Exoenzymes S, T, and Y in Systemic Spread of Pseudomonas aeruginosa PAO1 In Vivo journal February 2005
Pseudomonas aeruginosa Exhibits Sliding Motility in the Absence of Type IV Pili and Flagella journal December 2007

Cited By (17)

Microbial small molecules – weapons of plant subversion journal January 2018
Assembly and ecological function of the root microbiome across angiosperm plant species journal January 2018
Genome-wide identification of Pseudomonas syringae genes required for fitness during colonization of the leaf surface and apoplast journal September 2019
There is no hiding if you Seq: recent breakthroughs in Pseudomonas aeruginosa research revealed by genomic and transcriptomic next-generation sequencing journal February 2020
Discovery of Pantoea stewartii ssp. stewartii genes important for survival in corn xylem through a Tn-Seq analysis: Pantoea stewartii genes important in planta journal March 2018
Identification by Tn-seq of Dickeya dadantii genes required for survival in chicory plants: Dickeya dadantii genes important in planta journal November 2018
Insights to plant-microbe interactions provide opportunities to improve resistance breeding against root diseases in grain legumes: Microbe-supported resistance breeding in legumes journal July 2018
A Genome-Wide Screen Identifies Genes in Rhizosphere-Associated Pseudomonas Required to Evade Plant Defenses journal November 2018
Need for Laboratory Ecosystems To Unravel the Structures and Functions of Soil Microbial Communities Mediated by Chemistry journal July 2018
Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism journal February 2019
In vivo insertion pool sequencing identifies virulence factors in a complex fungal–host interaction journal April 2018
Disruption of microbial community composition and identification of plant growth promoting microorganisms after exposure of soil to rapeseed-derived glucosinolates journal July 2018
Unusual extracellular appendages deployed by the model strain Pseudomonas fluorescens C7R12 journal August 2019
Transposon-insertion sequencing screens unveil requirements for EHEC growth and intestinal colonization journal August 2019
Defining the Genetic Basis of Plant–Endophytic Bacteria Interactions journal April 2019
Functional genomics of lipid metabolism in the oleaginous yeast Rhodosporidium toruloides journal March 2018
Unearthing the Plant Growth-Promoting Traits of Bacillus megaterium RmBm31, an Endophytic Bacterium Isolated From Root Nodules of Retama monosperma journal February 2020