Using Genomes and Evolutionary Analyses to Screen for Host-Specificity and Positive Selection in the Plant Pathogen Xylella fastidiosa

Xylella fastidiosa infects several economically important crops in the Americas, and it also recently emerged in Europe. Here, using a set of Xylella genomes reflective of the genus-wide diversity, we performed a pan-genome analysis based on both core and accessory genes for two purposes: (i) to test associations between genetic divergence and plant host species and (ii) to identify positively selected genes that are potentially involved in arms-race dynamics. For the former, tests yielded significant evidence for the specialization of X. fastidiosa to plant host species. This observation contributes to a growing literature suggesting that the phylogenetic history of X. fastidiosa lineages affects the host range. For the latter, our analyses uncovered evidence of positive selection across codons for 5.3% (67 of 1,257) of the core genes and 5.4% (201 of 3,691) of the accessory genes. These genes are candidates to encode interacting factors with plant and insect hosts. Most of these genes had unknown functions, but we did identify some tractable candidates, including nagZ_2, which encodes a beta-glucosidase that is important for Neisseria gonorrhoeae biofilm formation; cya, which modulates gene expression in pathogenic bacteria, and barA, a membrane associated histidine kinase that has roles in cell division, metabolism, and pili formation. IMPORTANCE Xylella fastidiosa causes devasting diseases to several critical crops. Because X. fastidiosa colonizes and infects many plant species, it is important to understand whether the genome of X. fastidiosa has genetic determinants that underlie specialization to specific host plants. We analyzed genome sequences of X. fastidiosa to investigate evolutionary relationships and to test for evidence of positive selection on specific genes. We found a significant signal between genome diversity and host plants, consistent with bacterial specialization to specific plant hosts. By screening for positive selection, we identified both core and accessory genes that may affect pathogenicity, including genes involved in biofilm formation.