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Plant pathogens pose increasing threats to global food security, causing yield losses that exceed 30% in food-deficit regions. Xylella fastidiosa (Xf) represents the major transboundary plant pest and one of the world's most damaging pathogens in terms of socioeconomic impact. Spectral screening methods are critical to detect non-visual symptoms of early infection and prevent spread. However, the subtle pathogen-induced physiological alterations that are spectrally detectable are entangled with the dynamics of abiotic stresses. Here, using airborne spectroscopy and thermal scanning of areas covering more than one million trees of different species, infections and water stress levels, we reveal the existence of divergent pathogen- and host-specific spectral pathways that can disentangle biotic-induced symptoms. We demonstrate that uncoupling this biotic–abiotic spectral dynamics diminishes the uncertainty in the Xf detection to below 6% across different hosts. Assessing these deviating pathways against another harmful vascular pathogen that produces analogous symptoms, Verticillium dahliae, the divergent routes remained pathogen- and host-specific, revealing detection accuracies exceeding 92% across pathosystems. These urgently needed hyperspectral methods advance early detection of devastating pathogens to reduce the billions in crop losses worldwide. ; The study was partially funded by the European Union's Horizon 2020 Research and Innovation Programme through grant agreements POnTE (635646) and XF-ACTORS (727987), as well as by projects AGL2009-13105 from the Spanish Ministry of Education and Science, P08-AGR-03528 from the Regional Government of Andalusia and the European Social Fund, project E-RTA2017-00004-02 from 'Programa Estatal de I + D + I Orientada a los Retos de la Sociedad' of Spain and FEDER, Intramural Project 201840E111 from CSIC, and Project ITS2017-095 Consejeria de Medio Ambiente, Agricultura y Pesca de las Islas Baleares, Spain. The views expressed are purely those of the writers and may not in any circumstance be regarded as stating an official position of the European Commission.

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 (Pierce's 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.

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. ; This work was partially funded by projects XF-ACTORS (Xylella fastidiosa Active Containment Through a Multidisciplinary-Oriented Research Strategy; grant 727987 from the European Union's Horizon 2020 Framework Research Programme), 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), the Spanish olive oil Interprofesional and the Ministry of Agriculture, Fisheries and Food and the Project ITS2017-095 from 'Consejeria de Medio Ambiente, Agricultura y Pesca' from the Balearic Islands, Spain. M.P.V-A. was a recipient of a PhD fellowship from Intramural Project 201840E111 from CSIC.