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

Abstract

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.

Barrier effects on the spatial distribution of Xylella fastidiosa in Alicante, Spain

“…After the introduction of the pathogen with imported infected plant material, further spread in the area can also be driven by the movement of propagating plant material. Studies reconstructing the progression of almond leaf scorch disease in Majorca indicated that X. fastidiosa was introduced into this island with almond buds or stems from California, and then spread through the archipelago by grafting (Moralejo et al 2020). Grafting experiments performed in this study resulted in a transmission of about 15% with almond buds, but other studies reported values up to 60% and 80% with almond buds and stems, respectively (Mircetich et al 1976).…”

“…Grafting experiments performed in this study resulted in a transmission of about 15% with almond buds, but other studies reported values up to 60% and 80% with almond buds and stems, respectively (Mircetich et al 1976). In the case of Alicante, genetic studies indicated that X. fastidiosa might also have been introduced from California (Landa et al 2020). In the demarcated area in Alicante, almond groves were typically established with rootstock seeds that were later grafted on site with buds or stems of the scion (Cambra and Cambra 1991).…”

“…These grafting materials were generally obtained from almond trees in the area or from outside when a new cultivar was first introduced. In Barrier effects on Xylella distribution fact, previous studies suggested that the current extent of the pathogen had arisen from a single introduction (Cendoya et al 2020;Landa et al 2020). Nevertheless, with the information available, it is not possible to accurately trace back the movement of propagating plant material in the area and thus determine its actual role in the spread of X. fastidiosa.…”

“…multiplex ST81 and X. fastidiosa subsp. fastidiosa ST1 were introduced into the island of Majorca, Spain, with infected almond graftings from California, US (Moralejo et al 2020). Similarly, X. fastidiosa subsp.…”

“…Similarly, X. fastidiosa subsp. multiplex ST6 in Alicante, Spain, and Corsica, France, as well as ST87 from Tuscany, Italy, might have been introduced from California (Landa et al 2020). Human-assisted movement of infected insect vectors on plants or on their own as 'hitch-hikers' in vehicles can also disseminate X. fastidiosa, though information on these means of spread is limited (EFSA 2015).…”