The recent introductions of the bacterium Xylella fastidiosa (Xf) into Europe are linked to the international plant trade. However, both how and when these entries occurred remains poorly understood. Here, we show how almond scorch leaf disease, which affects ~79% of almond trees in Majorca (Spain) and was previously attributed to fungal pathogens, was in fact triggered by the introduction of Xf around 1993 and subsequently spread to grapevines (Pierceʼs disease). We reconstructed the progression of almond leaf scorch disease by using broad phylogenetic evidence supported by epidemiological data. Bayesian phylogenetic inference predicted that both Xf subspecies found in Majorca, fastidiosa ST1 (95% highest posterior density, HPD: 1990–1997) and multiplex ST81 (95% HPD: 1991–1998), shared their most recent common ancestors with Californian Xf populations associated with almonds and grapevines. Consistent with this chronology, Xf-DNA infections were identified in tree rings dating to 1998. Our findings uncover a previously unknown scenario in Europe and reveal how Pierce’s disease reached the continent.

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Xylella fastidiosa (Xf), the causal agent of Pierce's disease (PD), has long been considered a major threat to prosperous European viticulture. In May of 2017, PD was officially detected on a grapevine in Mallorca. To better understand the epidemiology of the first established outbreak of PD in Europe, the disease incidence and severity were assessed, vector transmission experiments were performed, and cultivar responses to Xf infections both in the field and in inoculation experiments were monitored. The genetic structure of Xf local populations was also investigated by multilocus sequence typing analysis, and their whole genome sequences and phylogenetic positions compared with respect to PD strains worldwide. Disease incidence was moderately low (0.07) and highly variable, ranging from 0.0 to 0.99. Its economic impact on wine production was considered low. Vineyards managed under conventional viticulture were significantly less infected than organic farming. Under greenhouse conditions, the insect Philaenus spumarius efficiently transmitted the pathogen from infected to healthy grapevines. In the inoculation experiments, Xf infected, to some degree, 29 of the 30 cultivar × rootstock combinations (n = 239). Cultivars Viura, Gorgollasa and Sauvignon Blanc were the most susceptible ones. All Xf isolates from grapevines belonged to sequence type ST1; they phylogenetically clustered within the Californian ST1 clade, with which they shared a 99.94% identity and the same plasmid. In addition, ST1 caused almond leaf scorch disease, where notably its incidence (0.78) and severity was much higher than PD. The likely reasons for these wide differences are discussed in the context of a 20‐year Xf introduction scenario.

Xylella fastidiosa (Xf) is a vascular plant pathogen native to the Americas. In 2013, it was first reported in Europe, implicated in a massive die-off of olive trees in Apulia, Italy. This finding prompted mandatory surveys across Europe, successively revealing that the bacterium was already established in some distant areas of the western Mediterranean. To date, the Balearic Islands (Spain) hold the major known genetic diversity of Xf in Europe. Since October 2016, four sequence types (ST) belonging to the subspecies fastidiosa (ST1), multiplex (ST7, ST81), and pauca (ST80) have been identified infecting 28 host species, including grapevines, almond, olive, and fig trees. ST1 causes Pierce’s disease (PD) and together with ST81 are responsible for almond leaf scorch disease (ALSD) in California, from where they were introduced into Mallorca in around 1993, very likely via infected almond scions brought for grafting. To date, almond leaf scorch disease affects over 81% of almond trees and Pierce’s disease is widespread in vineyards across Mallorca, although producing on average little economic impact. In this perspective, we present and analyze a large Xf-hosts database accumulated over four years of field surveys, laboratory sample analyses, and research to understand the underlying causes of Xf emergence and spread among crops and wild plants in the Balearic Islands. The impact of Xf on the landscape is discussed.

Xylella fastidiosa is a plant-pathogenic bacterium that causes serious diseases in many crops of economic importance and is a quarantine organism in the European Union. This study reports a de novo-assembled draft genome sequence of the first isolates causing Pierce’s disease in Europe: X. fastidiosa subsp. fastidiosa strains XYL1732/17 and XYL2055/17. Both strains were isolated from grapevines (Vitis vinifera) showing Pierce’s disease symptoms at two different locations in Mallorca, Spain. The XYL1732/17 genome is 2,444,109 bp long, with a G+C content of 51.5%; it contains 2,359 open reading frames and 48 tRNA genes. The XYL2055/17 genome is 2,456,780 bp long, with a G+C content of 51.5%; it contains 2,384 open reading frames and 48 tRNA genes.