Introduction and adaptation of an emerging pathogen to olive trees in Italy

The invasive plant pathogen Xylella fastidiosa currently threatens European flora through the loss of economically and culturallyimportant host plants. This emerging vector-bornebacterium, native to the Americas, causes several important diseasesin a wide range of plants including crops, ornamentals, and trees. Previously absent from Europe, and considered a quarantinepathogen, X. fastidiosa was first detected in Apulia, Italy in 2013 associated with a devastating disease of olive trees (Olive QuickDecline Syndrome, OQDS). OQDS has led to significant economic, environmental, cultural, as well as political crises. Althoughthe biology of X. fastidiosa diseases have been studied for over a century, there is still no information on the determinants ofspecificity between bacterial genotypes and host plant species, which is particularly relevant today as X. fastidiosa is expandingin the naive European landscape. We analysed the genomes of 79 X. fastidiosa samples from diseased olive trees acrossthe affected area in Italy as well as genomes of the most genetically closely related strains from Central America. We providedinsights into the ecological and evolutionary emergence of this pathogen in Italy. We first showed that the outbreak in Apuliais due to a single introduction from Central America that we estimated to have occurred in 2008 [95 % HPD: 1930-2016]. Byusing a combination of population genomic approaches and evolutionary genomics methods, we further identified a short listof genes that could play a major role in the adaptation of X. fastidiosa to this new environment. We finally provided experimentalevidence for the adaptation of the strain to this new environment