title: Enhanced in planta Fitness through Adaptive Mutations in EfpR, a Dual Regulator of Virulence and Metabolic Functions in the Plant Pathogen Ralstonia solanacearum.
abstract: Experimental evolution of the plant pathogen Ralstonia solanacearum, where bacteria were maintained on plant lineages for more than 300 generations, revealed that several independent single mutations in the efpR gene from populations propagated on beans were associated with fitness gain on bean. In the present work, novel allelic efpR variants were isolated from populations propagated on other plant species, thus suggesting that mutations in efpR were not solely associated to a fitness gain on bean, but also on additional hosts. A transcriptomic profiling and phenotypic characterization of the efpR deleted mutant showed that EfpR acts as a global catabolic repressor, directly or indirectly down-regulating the expression of multiple metabolic pathways. EfpR also controls virulence traits such as exopolysaccharide production, swimming and twitching motilities and deletion of efpR leads to reduced virulence on tomato plants after soil drenching inoculation. We studied the impact of the single mutations that occurred in efpR during experimental evolution and found that these allelic mutants displayed phenotypic characteristics similar to the deletion mutant, although not behaving as complete loss-of-function mutants. These adaptive mutations therefore strongly affected the function of efpR, leading to an expanded metabolic versatility that should benefit to the evolved clones. Altogether, these results indicated that EfpR is a novel central player of the R. solanacearum virulence regulatory network. Independent mutations therefore appeared during experimental evolution in the evolved clones, on a crucial node of this network, to favor adaptation to host vascular tissues through regulatory and metabolic rewiring.
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Anthony
authors.identifier: http://orcid.org/0000-0002-4473-3711
authors.initials: A
authors.lastname: Perrier
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Rémi
authors.initials: R
authors.lastname: Peyraud
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: David
authors.initials: D
authors.lastname: Rengel
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Xavier
authors.initials: X
authors.lastname: Barlet
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Emmanuel
authors.identifier: http://orcid.org/0000-0001-7616-9425
authors.initials: E
authors.lastname: Lucasson
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Jérôme
authors.initials: J
authors.lastname: Gouzy
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Nemo
authors.identifier: http://orcid.org/0000-0002-1802-0769
authors.initials: N
authors.lastname: Peeters
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Stéphane
authors.identifier: http://orcid.org/0000-0003-2498-2400
authors.initials: S
authors.lastname: Genin
authors.affiliation: LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
authors.forename: Alice
authors.identifier: http://orcid.org/0000-0001-5282-4157
authors.initials: A
authors.lastname: Guidot
mesh_terms: D020869:Gene Expression Profiling; D017343:Genes, Plant / Q000235:genetics*; D009154:Mutation; D010935:Plant Diseases / Q000382:microbiology*; D016133:Polymerase Chain Reaction; D043368:Ralstonia solanacearum / Q000235:genetics* / Q000378:metabolism* / Q000472:pathogenicity*; D014774:Virulence / Q000235:genetics*; D037521:Virulence Factors / Q000378:metabolism
chemical_list: D037521:Virulence Factors