Diverse mobile genetic elements shaped the evolution of Streptomyces virulence.

Mobile genetic elements can innovate bacteria with new traits. In plant pathogenic Streptomyces, frequent and recent acquisition of integrative and conjugative or mobilizable genetic elements is predicted to lead to the emergence of new lineages that gained the capacity to synthesize Thaxtomin, a phytotoxin neccesary for induction of common scab disease on tuber and root crops. Here, we identified components of the Streptomyces-potato pathosystem implicated in virulence and investigated them as a nested and interacting system to reevaluate evolutionary models. We sequenced and analysed genomes of 166 strains isolated from over six decades of sampling primarily from field-grown potatoes. Virulence genes were associated to multiple subtypes of genetic elements differing in mechanisms of transmission and evolutionary histories. Evidence is consistent with few ancient acquisition events followed by recurrent loss or swaps of elements carrying Thaxtomin A-associated genes. Subtypes of another genetic element implicated in virulence are more distributed across Streptomyces. However, neither the subtype classification of genetic elements containing virulence genes nor taxonomic identity was predictive of pathogenicity on potato. Last, findings suggested that phytopathogenic strains are generally endemic to potato fields and some lineages were established by historical spread and further dispersed by few recent transmission events. Results from a hierarchical and system-wide characterization refine our understanding by revealing multiple mechanisms that gene and bacterial dispersion have had on shaping the evolution of a Gram-positive pathogen in agricultural settings.

The Phytotoxin Thaxtomin A Is the Primary Virulence Determinant for Scab Disease of Beet, Carrot, and Radish Caused by Streptomyces scabiei.

Several species of Streptomyces cause common scab, a major disease of potato, primarily through the phytotoxic effects of the phytotoxin thaxtomin A. Several phytopathogenic Streptomyces species have also been implicated as the causative agents of scab diseases of taproot crops including beet, carrot, radish, parsnip, and turnip. But the molecular mechanisms employed by Streptomyces to infect these crops is unknown. In this work, we tested the hypothesis that thaxtomin A biosynthesis is also necessary for Streptomyces-caused scab of beet, carrot, radish, and turnip. Thaxtomin A induced plant stunting and cell death of all four of these species. Streptomyces mutants in which the transcriptional regulator of thaxtomin A biosynthesis is disrupted were nonvirulent on all four crops, and complementation of the transcriptional regulator rescued thaxtomin A biosynthesis and plant pathogenicity to wild-type levels. These results demonstrate that thaxtomin A is the primary virulence determinant of scab disease of these other crops.

A Novel Species-Level Group of Streptomyces Exhibits Variation in Phytopathogenicity Despite Conservation of Virulence Loci.

The genus Streptomyces includes several phytopathogenic species that cause common scab, a devastating disease of tuber and root crops, in particular potato. The diversity of species that cause common scab is unknown. Likewise, the genomic context necessary for bacteria to incite common scab symptom development is not fully characterized. Here, we phenotyped and sequenced the genomes of five strains from a poorly studied Streptomyces lineage. These strains form a new species-level group. When genome sequences within just these five strains are compared, there are no polymorphisms of loci implicated in virulence. Each genome contains the pathogenicity island that encodes for the production of thaxtomin A, a phytotoxin necessary for common scab. Yet, not all sequenced strains produced thaxtomin A. Strains varied from nonpathogenic to highly virulent on two hosts. Unexpectedly, one strain that produced thaxtomin A and was pathogenic on radish was not aggressively pathogenic on potato. Therefore, while thaxtomin A biosynthetic genes and production of thaxtomin A are necessary, they are not sufficient for causing common scab of potato. Additionally, results show that even within a species-level group of Streptomyces strains, there can be aggressively pathogenic and nonpathogenic strains despite conservation of virulence genes.

Cultivar Resistance to Common Scab Disease of Potato Is Dependent on the Pathogen Species.

Common scab of potato is a superficial tuber disease caused by Streptomyces species that produce the phytotoxin thaxtomin. Because common scab development is highly dependent on the effects of this single toxin, the current operating paradigm in common scab pathology is that a potato cultivar resistant to one strain of the common scab pathogen is resistant to all strains. However, cultivar resistance to common scab disease identified in one breeding program is often not durable when tested in other potato breeding programs across the United States. We infected 55 potato cultivar populations with three distinct species of the common scab pathogen and identified cultivars that were resistant or susceptible to all three species and cultivars that had widely varying resistance dependent on the pathogen species. Overall lower virulence was associated with the strain that produces the least thaxtomin. This result showcases several cultivars of potato that are expected to be resistant to the majority of common scab populations but also highlights that many potato cultivars are resistant to only specific species of the pathogen. These results demonstrate that extension specialists and growers must consider their local population of the common scab pathogen when selecting which cultivars to plant for common scab resistance.