Effector loss and gain drives pathogen host range at a fitness cost

Epidemic preparedness depends on tracking microbial evolution that drives shifts in ecological behaviors such as disease emergence. However, the genetic constraints for microbial host adaptation to emerge for generalist and specialist behaviors remain poorly described. Here, we show that generalist cereal pathogen Xanthomonas translucens arose from a specialist ancestor via the loss of a single effector gene, xopAL1. Deleting barley-specialist X. translucens xopAL1 recapitulated the host jump to wheat and demonstrates risk across each globally distributed genetic lineage. However, this niche expansion via XopAL1 loss incurs a significant pathogenic fitness cost to colonize barley. Moreover, the specialist lineage gained an additional effector gene, xopAJ, which enhanced virulence on barley while restricting oat infection, thereby reinforcing niche specialization. We further identified key host pathways mediating resistance to the specialist lineage of X. translucens, opening avenues for potentially identifying targets for crop improvement. Our work provides an experimentally validated evolutionary framework to understand mechanisms of intergenera host jump. Overall, we demonstrate that single events of gene loss and gain shape ecological behaviors of pathogens by creating a dynamic trade-off between niche breadth and specialization.