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

Abstract

AbstractClavibacter, 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. michiganensispopulations 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 ofClavibacterin wild and commercial tomato cultivars, providing evolutionary insights that informed on the pathogenicity of this phytopathogen. Unexpectedly, our phylogeny situate the last common ancestor ofC. michiganensisnext toClavibacterisolates from grasses rather than to the sole strain we could isolate from wild tomato, which is closer toC. capsiciassociated with pepper. Pathogenicity profiling of selectedC. michiganensisisolates, together withC. phaseoliandC. californiensisas sister taxa of the grass clade, and the newly isolatedC. capsicifrom 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 ofC. 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 ofC. michiganensiswith pathogenicity factors that remain to be characterized.