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

Anthony Perrier,Jérôme Gouzy,Rémi Peyraud,Emmanuel Lucasson,David Rengel,Xavier Barlet,Alice Guidot,Nemo Peeters,Stéphane Genin,Darrell Desveaux

doi:10.1371/journal.ppat.1006044

Anthony Perrier, Jérôme Gouzy + Show 8 more

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

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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.

Highlights

Bacterial plant pathogens constitute a major threat to crop production
During an evolution experiment of R. solanacearum, where bacteria were maintained on plant lineages for more than 300 generations, we demonstrated that several single mutations in the regulatory gene efpR were associated with fitness gain on plants
We investigated whether mutations in efpR occurred in populations evolved in plant species other than bean

Summary

Introduction

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]. R. solanacearum is a soilborne pathogen that infects the plants through the roots, invades the xylem vessels and spreads to aerial parts of the plant through the vascular system where it multiplies extensively and produces large amounts of exopolysaccharide (EPS) [9]. To cope with these various soil and plant microenvironments, R. solanacearum has evolved a complex regulatory network that senses key signals and triggers important physiological changes via global shifts in gene expression [10]. At the center of this virulence regulatory network is the global regulator PhcA, a LysR-type transcriptional regulator that controls expression of many genes [11]

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