The bacterium Xylella fastidiosa re-emerged as a plant pathogen of global importance in 2013 when it was first associated with an olive tree disease epidemic in Italy. The current threat to Europe and the Mediterranean basin, as well as other world regions, has increased as multiple X. fastidiosa genotypes have now been detected in Italy, France, and Spain. Although X. fastidiosa has been studied in the Americas for more than a century, there are no therapeutic solutions to suppress disease development in infected plants. Furthermore, because X. fastidiosa is an obligatory plant and insect vector colonizer, the epidemiology and dynamics of each pathosystem are distinct. They depend on the ecological interplay of plant, pathogen, and vector and on how interactions are affected by biotic and abiotic factors, including anthropogenic activities and policy decisions. Our goal with this review is to stimulate discussion and novel research by contextualizing available knowledge on X. fastidiosa and how it may be applicable to emerging diseases.

Following a request from the European Commission, the EFSA Plant Health Panel updated its pest categorisation of Xylella fastidiosa, previously delivered as part of the pest risk assessment published in 2015. X. fastidiosa is a Gram‐negative bacterium, responsible for various plant diseases, including Pierce's disease, phony peach disease, citrus variegated chlorosis, olive quick decline syndrome, almond leaf scorch and various other leaf scorch diseases. The pathogen is endemic in the Americas and is present in Iran. In the EU, it is reported in southern Apulia in Italy, on the island of Corsica and in the Provence‐Alpes‐Côte d'Azur region in France, as well as in the Autonomous region of Madrid, the province of Alicante and the Balearic Islands in Spain. The reported status is ‘transient, under eradication’, except for the Balearic Islands, Corsica and southern of Apulia, where the status is ‘present with a restricted distribution, under containment’. The pathogen is regulated under Council Directive 2000/29/EC and through emergency measures under http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32015D0789 (as amended http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32017D2352). The pest could enter the EU via host plants for planting and via infectious insect vectors. The host range includes hundreds of host species listed in the EFSA host plant database. In the EU, host plants are widely distributed and climatic conditions are favourable for its establishment. X. fastidiosa can spread by movement of host plants for planting and infectious insect vectors. X. fastidiosa is known to cause severe direct damage to major crops including almonds, citrus, grapevines, olives, stone fruits and also forest trees, landscape and ornamental trees, with high impacts. The criteria assessed by the Panel for consideration as a potential Union quarantine pest are met (the pathogen is present in the EU, but it has a restricted distribution and is under official control). X. fastidiosa is not considered as a regulated non‐quarantine pest (RNQP) as the pathogen may spread also via insect vector transmission.

Xylella fastidiosa is a plant-pathogenic bacterium recently introduced in Europe that is causing decline in olive trees in the South of Italy. Genetic studies have consistently shown that the bacterial genotype recovered from infected olive trees belongs to the sequence type ST53 within subspecies pauca. This genotype, ST53, has also been reported to occur in Costa Rica. The ancestry of ST53 was recently clarified, showing it contains alleles that are monophyletic with those of subsp. pauca in South America. To more robustly determine the phylogenetic placement of ST53 within X. fastidiosa, we performed a comparative analysis based on single nucleotide polymorphisms (SNPs) and the study of the pan-genome of the 27 currently public available whole genome sequences of X. fastidiosa. The resulting maximum-parsimony and maximum likelihood trees constructed using the SNPs and the pan-genome analysis are consistent with previously described X. fastidiosa taxonomy, distinguishing the subsp. fastidiosa, multiplex, pauca, sandyi, and morus. Within the subsp. pauca, the Italian and three Costa Rican isolates, all belonging to ST53, formed a compact phylotype in a clade divergent from the South American pauca isolates, also distinct from the recently described coffee isolate CFBP8072 imported into Europe from Ecuador. These findings were also supported by the gene characterization of a conjugative plasmid shared by all the four ST53 isolates. Furthermore, isolates of the ST53 clade possess an exclusive locus encoding a putative ATP-binding protein belonging to the family of histidine kinase-like ATPase gene, which is not present in isolates from the subspecies multiplex, sandyi, and pauca, but was detected in ST21 isolates of the subspecies fastidiosa from Costa Rica. The clustering and distinctiveness of the ST53 isolates supports the hypothesis of their common origin, and the limited genetic diversity among these isolates suggests this is an emerging clade within subsp. pauca.

TitleNatural competence rates are variable among xylella fastidiosa strains and homologous recombination occurs in vitro between subspecies fastidiosa and multiplex Xylella fastidiosa, an etiological agent of emerging crop diseases around the world, is naturally competent for the uptake of DNA from the environment that is incorporated into its genome by homologous recombination. Homologous recombination between subspecies of X. fastidiosa was inferred by in silico studies and was hypothesized to cause disease emergence. However, no experimental data are available on the degree to which X. fastidiosa strains are capable of competence and whether recombination can be experimentally demonstrated between subspecies. Here, using X. fastidiosa strains from different subspecies, natural competence in 11 of 13 strains was confirmed with plasmids containing antibiotic markers flanked by homologous regions and, in three of five strains, with dead bacterial cells used as source of donor DNA. Recombination frequency differed among strains and was correlated to growth rate and twitching motility. Moreover, intersubspecific recombination occurred readily between strains of subsp. fastidiosa and multiplex, as demonstrated by movement of antibiotic resistance and green fluorescent protein from donor to recipient cells and confirmed by DNA sequencing of the flanking arms of recombinant strains. Results demonstrate that natural competence is widespread among X. fastidiosa strains and could have an impact in pathogen adaptation and disease development.