Adaptative and ancient co-evolution of integrons with Xanthomonas genomes

Integrons are genetic elements that facilitate gene acquisition. They have been extensively studied in clinical bacteria, but their evolutionary role in phytopathogens remains underexplored. Here, we analysed complete genomes of Xanthomonas species to investigate the origin, distribution and functional dynamics of integrons in this genus. We found that 93% of genomes harboured integrons. The integron-integrase gene intI was predominantly located downstream of ilvD, indicating an ancestral acquisition of integrons, predating diversification within the genus. Phylogenetic analyses support vertical inheritance of intI, with the exception of rare horizontal gene transfer events, notably in Xanthomonas arboricola. Despite their widespread presence, full-length intI genes and active integron platforms are only retained in some species, especially Xanthomonas campestris, which shows high integron gene cassette variability and functional integron activity. In contrast, species such as Xanthomonas cissicola and Xanthomonas phaseoli exhibit widespread intI inactivation, likely occurring early in their divergence, leading to more stable cassette arrays and conserved integron-associated phenotypes. The number and diversity of genes within cassette arrays varied significantly by species and, to a lesser extent, by the ecological context of plant host cultivation. While most cassettes encoded proteins without a known function, those with annotated roles were associated with stress response mechanism, competitive exclusion and plant-associated functions. Together, our findings demonstrate that integrons in Xanthomonas likely originated from a single ancient acquisition event, preceding genus-wide speciation, and have co-evolved with Xanthomonas pathovars as they adapted to distinct plant hosts.