The genus Dickeya comprises plant pathogens that cause diseases in a large range of economically important crops and ornamentals. Strains previously assigned to the species Dickeya zeae are major pathogens attacking vital crops such as maize and rice. They are also frequently isolated from surface water. The newly described species Dickeya oryzae is closely related to D. zeae members, so that the limit between the two species can be difficult to define. In order to clearly distinguish the two species, globally described by the term ‘ D. zeae complex’, we sequenced the genome of four new water isolates and compared them to 14 genomes available in databases. Calculation of average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) values confirmed the phylogenomic classification into the two species D. zeae and D. oryzae . It also allowed us to propose a new species, Dickeya parazeae sp. nov., to characterize a clade distinct from those containing the D. zeae type strain NCPPB2538^T. Strain S31^T (CFBP 8716^T=LMG 32070^T) isolated from water in France is proposed as the type strain of the new species. Phenotypic analysis of eight publically available strains revealed traits common to the five tested D. oryzae members but apparently not shared by the D. oryzae type strain. Genomic analyses indicated that a simple distinction between the species D. zeae , D. parazeae and D. oryzae can be obtained on the basis of the recA sequence. D. oryzae can be distinguished from the two other species by growth on l-tartaric acid. Based on the recA marker, several strains previously identified as D. zeae were re-assigned to the species D. parazeae or D. oryzae . This study also highlighted the broad host range diversity of these three species.

The pectinolytic enterobacteria of the Pectobacterium and Dickeya genera are causative agents of maceration-associated diseases affecting a wide variety of crops and ornamentals. For the past decade, the emergence of a novel species D. solani was observed in potato fields in Europe and the Mediterranean basin. The purpose of this study is to search by comparative genomics the genetic traits that could be distinctive to other Dickeya species and be involved in D. solani adaptation to the potato plant host.

Summary: Successful infection of a pathogen relies on the coordinated expression of numerous virulence factor‐encoding genes. In plant–bacteria interactions, this control is very often achieved through the integration of several regulatory circuits controlling cell–cell communication or sensing environmental conditions. Dickeya dadantii (formerly Erwinia chrysanthemi ), the causal agent of soft rot on many crops and ornamentals, provokes maceration of infected plants mainly by producing and secreting a battery of plant cell wall‐degrading enzymes. However, several other virulence factors have also been characterized. During Arabidopsis infection, most D. dadantii virulence gene transcripts accumulated in a coordinated manner during infection. This activation requires a functional GacA–GacS two‐component regulatory system but the Gac system is not involved in the growth phase dependence of virulence gene expression. Here we show that, contrary to Pectobacterium , the AHL‐mediated ExpIR quorum‐sensing system does not play a major role in the growth phase‐dependent control of D. dadantii virulence genes. On the other hand, the global regulator PecS participates in this coordinated expression since, in a pecS mutant, an early activation of virulence genes is observed both in vitro and in planta . This correlated with the known hypervirulence phenotype of the pecS mutant. Analysis of the relationship between the regulatory circuits governed by the PecS and GacA global regulators indicates that these two regulators act independently. PecS prevents a premature expression of virulence genes in the first stages of colonization whereas GacA, presumably in conjunction with other regulators, is required for the activation of virulence genes at the onset of symptom occurrence.