Allopatric Plant Pathogen Population Divergence following Disease Emergence

Within the landscape of globally distributed pathogens, populations differentiate via both adaptive and nonadaptive forces. Individual populations are likely to show unique trends of genetic diversity, host-pathogen interaction, and ecological adaptation. In plant pathogens, allopatric divergence may occur particularly rapidly within simplified agricultural monoculture landscapes. As such, the study of plant pathogen populations in monocultures can highlight the distinct evolutionary mechanisms that lead to local genetic differentiation. Xylella fastidiosa is a plant pathogen known to infect and damage multiple monocultures worldwide. One subspecies, Xylella fastidiosa subsp. fastidiosa, was first introduced to the United States ∼150 years ago, where it was found to infect and cause disease in grapevines (Pierce's disease of grapevines, or PD). Here, we studied PD-causing subsp. fastidiosa populations, with an emphasis on those found in the United States. Our study shows that following their establishment in the United States, PD-causing strains likely split into populations on the East and West Coasts. This diversification has occurred via both changes in gene content (gene gain/loss events) and variations in nucleotide sequence (mutation and recombination). In addition, we reinforce the notion that PD-causing populations within the United States acted as the source for subsequent subsp. fastidiosa outbreaks in Europe and Asia.IMPORTANCE Compared to natural environments, the reduced diversity of monoculture agricultural landscapes can lead bacterial plant pathogens to quickly adapt to local biological and ecological conditions. Because of this, accidental introductions of microbial pathogens into naive regions represents a significant economic and environmental threat. Xylella fastidiosa is a plant pathogen with an expanding host and geographic range due to multiple intra- and intercontinental introductions. X. fastidiosa subsp. fastidiosa infects and causes disease in grapevines (Pierce's disease of grapevines [PD]). This study focused on PD-causing X. fastidiosa populations, particularly those found in the United States but also invasions into Taiwan and Spain. The analysis shows that PD-causing X. fastidiosa has diversified via multiple cooccurring evolutionary forces acting at an intra- and interpopulation level. This analysis enables a better understanding of the mechanisms leading to the local adaptation of X. fastidiosa and how a plant pathogen diverges allopatrically after multiple and sequential introduction events.