A host shift as the origin of tomato bacterial canker caused by Clavibacter michiganensis

Clavibacter, a plant endophytic actinobacterial genus, includes phytopathogens with devasting effects on several crops. C. michiganensis, the seed-borne and causal agent of bacterial canker in tomato, is arguably the most notorious species of the genus. Yet, its origin and natural reservoirs remain elusive. Moreover, C. michiganensis populations show different genetic pathogenicity profiles with equally unpredictable plant disease outcomes. To tackle these uncertainties, here we analyze genomic data generated during a decade-long survey of Clavibacter in wild and commercial tomato cultivars, providing evolutionary insights that informed on the pathogenicity of this phytopathogen. Unexpectedly, our phylogeny situate the last common ancestor of C. michiganensis next to Clavibacter isolates from grasses rather than to the sole strain we could isolate from wild tomato, which is closer to C. capsici associated with pepper. Pathogenicity profiling of selected C. michiganensis isolates, together with C. phaseoli and C. californiensis as sister taxa of the grass clade, and the newly isolated C. capsici from wild tomato, was found to be congruent with the proposed phylogenetic relationships. Furthermore, we identified gene enrichment after an evolutionary bottleneck leading to the appearance of C. michiganesis, including known pathogenicity factors but also hitherto unnoticed genes with such potential, i.e., nutrient acquisition and specialized metabolite metabolic gene clusters. The holistic perspective provided by our long-term and in-depth analyses hints towards a host shift event as the origin of the causative agent of bacterial canker in tomato, leading to a complex of C. michiganensis with pathogenicity factors that remain to be characterized.