Research Article: Enhanced in planta Fitness through Adaptive Mutations in EfpR, a Dual Regulator of Virulence and Metabolic Functions in the Plant Pathogen Ralstonia solanacearum

Date Published: December 2, 2016

Publisher: Public Library of Science

Author(s): Anthony Perrier, Rémi Peyraud, David Rengel, Xavier Barlet, Emmanuel Lucasson, Jérôme Gouzy, Nemo Peeters, Stéphane Genin, Alice Guidot, Darrell Desveaux.

http://doi.org/10.1371/journal.ppat.1006044

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.

Partial Text

Bacterial plant pathogens constitute a major threat to crop production. In addition, disease emergence can occur through rapid adaptation of many pathogens to new hosts [1,2]. Understanding how pathogens are adapting to new hosts is crucial for unraveling the mechanisms that drive disease emergence. One way to study evolution of pathogen adaptation to new hosts is to conduct experimental evolution of the pathogen in a given host over hundreds of generations [3–6]. The combination of experimental evolution with whole-genome sequencing has enabled the characterization of the mutations underlying the within-host fitness gain in various host-pathogen systems [4,6].

In this work, we investigated the role of the efpR gene, a gene involved in adaptation of R. solanacearum to various host plants, discovered during an experimental evolution where bacteria were maintained on plant lineages for more than 300 generations [6]. This former study showed that the fitness gain of the evolved bacteria was associated to SNPs within the efpR sequence. A similar fitness gain was obtained by deleting efpR. In the present study, we provide evidence that EfpR is mainly a repressor of gene expression (60% of the DEGs), suggesting that the mutations in efpR selected during the experimental evolution led to the de-repression of biological functions contributing to the observed fitness gain. Indeed, our data showed that EfpR regulates, directly or indirectly, a large number of genes (about 17% of the WT genes displayed a differential expression in the ΔefpR mutant). As a consequence, EfpR controls many metabolic pathways and virulence-associated traits. Similar changes in global gene expression through mutations affecting regulatory network components have been observed in evolution experiments conducted with bacteria and appear to be a first and rapid adaptive response to novel environmental conditions [18].

 

Source:

http://doi.org/10.1371/journal.ppat.1006044

 

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