Insights into the epidemiology of Pierce's disease in vineyards of Mallorca, Spain

Abstract

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.

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

“…fastidiosa ST1, collected from Majorca, reported the 38 kb plasmid pXFAS_5235, with the highest sequence similarities to the conjugative plasmid pXFAS01 from isolate M23 causing ALSD in California 39,42 . In addition, a close genetic relationship between Majorcan Xf isolates belonging to ST1 and ST81 and Californian Xf isolates related to Pierce's disease and ALSD was confirmed recently by phylogenetic analysis based on core genomes 6,31 .…”

“…As expected, the orchards closest to the putative main focus area (radius < 20 km) and therefore with a longer exposure time to Xf showed a higher incidence (χ = 25.21, df = 1, P = 0.0001; Supplementary Data 1) and mortality (χ = 26.49, df = 1, P = 0.0001; Supplementary Data 1), supporting the hypothesis that Son Carrió was an expanding focus. Likewise, the incidence and severity of Pierce's disease had previously been shown to be higher in orchards closer to the main propagation centre in Son Carrió 6 . To further capture the spatial-temporal spread of ALSD, we mapped the estimated disease incidence (%) and mortality (%) distribution among orchards for 2012 and 2017 using QGIS 48 geographic information system software ( Fig.…”

“…Although no etiological agent was ascribed, this disease was associated with a complex of fungal trunk pathogens 2,3 and their interactions with known disease-predisposing factors such as prolonged drought and tree aging 4,5 . This early disease diagnosis, however, was recently challenged after the detection of Xylella fastidiosa (Xf) in Majorca in October 2016 6 . More than 119 almond samples tested positive for Xf in a 2017 analysis conducted by the Balearic Islands Official Plant Health Laboratory (LOSVIB), which raised suspicion that Xf could underlie the sudden emergence of this unprecedented disease 7 .…”

“…n°: CP052855.1) recovered from an olive tree in California. Both ST1 and ST81 were well distributed across the island, with ST81 also infecting the widespread wild olive trees among other hosts, whereas strain ST1 caused Pierce's disease as well 6 . No clear spatial pattern in their distribution was observed, suggesting long-term spread and mixed-infection scenarios ( Supplementary Fig.…”

“…ALSD is transmitted by spittlebugs. Based on 'olive quick decline syndrome' epidemiological studies in Italy 21 and Pierce's disease in Majorca 6 , P. spumarius was the main candidate vector for ALSD. In the transmission experiment, P. spumarius adults reared from nymphs and caged on ALSD symptomatic trees vectored Xf to healthy almond saplings.…”