Phylogenetic inference enables reconstruction of a long-overlooked outbreak of almond leaf scorch disease (Xylella fastidiosa) in Europe

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.This work was partially funded by projects XF-ACTORS (Xylella fastidiosa Active Containment Through a Multidisciplinary-Oriented Research Strategy; grant 727987 from European Union’s Horizon 2020 Framework Research Programme) and ERTA2017-00004-02 and E-RTA2017-00004-04 (Desarrollo de estrategias de erradicación, contención y control de X. fastidiosa en España) from ‘Programa Estatal de I + D + I Orientada a los Retos de la Sociedad of the Spanish Government’ and FEDER) and from the Organización Profesional del Aceite de Oliva Español’. M.P.V-A. was recipient of a PhD fellowship from Intramural Project 201840E111from CSIC. A.B. was recipient of a postdoctoral UIB contract funded by the Vicerectorado de Investigación e Internacionalización of the University of the Balearic Islands