Agrobacterium tumefaciens fitness genes involved in the colonization of plant tumors and roots

Abstract

Summary Agrobacterium tumefaciens colonizes the galls (plant tumors) it causes, and the roots of host and nonhost plants. Transposon‐sequencing (Tn‐Seq) was used to discover A.tumefaciens genes involved in reproductive success (fitness genes) on Solanum lycopersicum and Populus trichocarpa tumors and S.lycopersicum and Zea mays roots. The identified fitness genes represent 3–8% of A. tumefaciens genes and contribute to carbon and nitrogen metabolism, synthesis and repair of DNA, RNA and proteins and envelope‐associated functions. Competition assays between 12 knockout mutants and wild‐type confirmed the involvement of 10 genes (trpB, hisH, metH, cobN, ntrB, trxA, nrdJ, kamA, exoQ, wbbL) in A.tumefaciens fitness under both tumor and root conditions. The remaining two genes (fecA, noxA) were important in tumors only. None of these mutants was nonpathogenic, but four (hisH, trpB, exoQ, ntrB) exhibited impaired virulence. Finally, we used this knowledge to search for chemical and biocontrol treatments that target some of the identified fitness pathways and report reduced tumorigenesis and impaired establishment of A.tumefaciens on tomato roots using tannic acid or Pseudomonas protegens, which affect iron assimilation. This work revealed A.tumefaciens pathways that contribute to its competitive survival in plants and highlights a strategy to identify plant protection approaches against this pathogen.

A Comprehensive Overview of the Genes and Functions Required for Lettuce Infection by the Hemibiotrophic Phytopathogen Xanthomonas hortorum pv. vitians

“… b Genes required for R. solanacearum fitness in tomato plants according to Su et al ( 32 ). c Genes required for A. fabrum fitness under at least one condition (i.e., tomato tumors, tomato roots, maize roots, or poplar tumors) according to Torres et al ( 33 ). d Genes required for D. dadantii fitness in chicory leaves according to Royet et al ( 29 ).…”

“… c Genes required for A. fabrum fitness under at least one condition (i.e., tomato tumors, tomato roots, maize roots, or poplar tumors) according to Torres et al ( 33 ). …”

“…Similar studies have been conducted on a handful of other plant-pathogenic bacteria in planta in the past 3 years, allowing us to compare the gene set we identified with those unveiled by other similar studies. We searched for homologs of the genes we identified in the data sets obtained for D. dadantii in chicory leaves ( 29 ), P. syringae in bean leaves ( 30 ), R. solanacearum in tomato roots ( 32 ), and A. fabrum under multiple conditions (tomato tumors and roots, maize roots, and poplar tumors) ( 33 ).…”

“…For the plant-pathogenic species Pantoea stewartii subsp. stewartii ( 28 ), Dickeya dadantii ( 29 ), Pseudomonas syringae ( 30 , 31 ), Ralstonia solanacearum ( 32 ), and Agrobacterium tumefaciens ( 33 ), Tn-seq provided an overall picture of the cellular functions and processes mobilized during plant infection and identified novel virulence factors.…”

Genome-wide identification of fitness determinants in theXanthomonas campestrisbacterial pathogen during early stages of plant infection

“…Such TnSeq approaches have been widely used to study animal pathogens and have led to the discovery of infectious processes including virulence factors, genes required for transmission between hosts or antibiotic resistance (reviewed in Cain et al, 2020; van Opijnen and Levin, 2020) but have only recently been applied to plant pathogens. To date, TnSeq screens of genes contributing to in planta fitness have been performed in Pantoea stewartii (on corn; Duong et al, 2018), Dickeya dadantii (on chicory; Royet et al, 2019), Agrobacterium tumefaciens (on tomato; (Gonzalez-Mula et al, 2019; Torres et al, 2022) and Pseudomonas syringae (on bean and pepper; Helmann et al, 2019; Helmann et al, 2020). While these studies provided diverse insights specific to each pathosystem, they all highlighted the importance of metabolic capacities and secretion systems for optimal growth in planta .…”