Key words: disease emergence, evolution of aggressiveness in agro-ecosystem, host plant specialization, host shift, plant-pathogen interaction, Plasmopara viticola (the causal agent of grapevine downy mildew), quantitative adaptation to cultivar, Vitis vinifera and wild relatives. SummaryAssortative mating resulting from host plant specialization has been proposed to facilitate rapid ecological divergence in biotrophic plant pathogens. Downy mildews, a major group of biotrophic oomycetes, are prime candidates for testing speciation by host plant specialization.Here, we combined a phylogenetic and morphological approach with cross-pathogenicity tests to investigate host plant specialization and host range expansion in grapevine downy mildew. This destructive disease is caused by Plasmopara viticola, an oomycete endemic to North America on wild species and cultivated grapevines.Multiple genealogies and sporangia morphology provide evidence that P. viticola is a complex of four cryptic species, each associated with different host plants. Cross-inoculation experiments showed complete host plant specialization on Parthenocissus quinquefolia and on Vitis riparia, whereas cryptic species found on V. aestivalis, V. labrusca and V. vinifera were revealed to be less specific. We reconstructed the recent host range expansion of P. viticola from wild to cultivated grapevines, and showed that it was accompanied by an increase in aggressiveness of the pathogen.This case study on grapevine downy mildew illustrates how biotrophic plant pathogens can diversify by host plant specialization and emerge in agrosystems by shifting to cultivated hosts. These results might have important implications for viticulture, including breeding for resistance and disease management.

Lecomte, P., Darrieutort, G., Liminana, J.-M., Comont, G., Muruamendiaraz, A., Legorburu, F.-J., Choueiri, E., Jreijiri, F., El Amil, R., and Fermaud, M. 2012. New insights into esca of grapevine: The development of foliar symptoms and their association with xylem discoloration Plant Dis. 96:924-934.A new study on the development of foliar symptoms of esca was carried out from 2004 to 2006 in five mature vineyards in Aquitaine, France. Symptoms were monitored for severity and changes over time. Initial foliar symptoms were characterized by the presence of drying zones or discolorations (reddening or yellowing), which are symptoms that have also been attributed to Black Dead Arm (BDA). Then, the less-severely affected leaves persisted throughout the summer and developed into typical "tiger-stripe" symptoms of esca. The most severely symptomatic leaves fell soon after symptoms appeared. Severely diseased vines showed typical apoplectic or acute forms of esca that did not differ from the severe BDA forms. The appearance of leafsymptomatic vines increased uniformly over time, reaching a maximum incidence by the end of July. A second survey in 41 European and Lebanese vineyards showed that longitudinal discolorations were visible under the bark of 95% of the vines showing foliar esca symptoms. These wood symptoms, also previously attributed to BDA, appeared as xylem orange-brown stripes. Thus, foliar symptoms of esca showed transitory phases which overlapped with some BDA descriptions. Most of these symptoms, in the west-palearctic regions that were investigated, were commonly associated with the presence of one or several xylem discolorations.

Botryosphaeriaceae is a fungal family comprising many species involved in botryosphaeria dieback, a worldwide grapevine trunk disease. Currently, the interactions between Botryosphaeriaceae species and various grapevine cultivars are poorly understood and little data is available. This study investigated various life traits of five isolates belonging to four species of Botryosphaeriaceae found in French vineyards (Diplodia mutila, Diplodia seriata, Lasiodiplodia viticola and Neofusicoccum parvum). The two species N. parvum and L. viticola exhibited the highest optimal growth temperature and the best growth rates. They were also responsible for the most extensive necrosis and cankers in three Vitis vinifera cultivars (Cabernet Sauvignon, Merlot and Ugni-Blanc) that differed in susceptibility to botryosphaeria dieback, and in two genotypes resistant to downy and powdery mildew (RV4 and RV5). Identification of the extracellular toxins produced by isolates in culture media showed that the N. parvum isolate had a different metabolite profile from the others, producing terremutin and salicylic acid derivatives, which are known to be compounds associated with virulence. In a second step, life traits were associated with nondestructive monitoring of gene expression involved in the defence mechanisms of five grapevine cultivars and genotypes after inoculation of wood cuttings with Botryosphaeriaceae. The transcript analyses were carried out at different times and were associated with principal component analysis (PCA). Each cultivar presented a specific transcript signature and several transcripts were correlated either with the size of necrosis/cankers or with symptom reduction, thus offering useful markers for breeding or estimating the defence status of plants.

Phaeomoniella chlamydospora, (Chaetothyriales, Herpotrichiellaceae) is one of the main causal agents of Petri disease and esca on grapevines. We have used AFLP markers to study the population genetic structure of 74 isolates collected at different spatial scales: 56 isolates originated from vines with esca disease sampled from four French vineyards (Poitou-Charentes, Aquitaine, Languedoc-Roussillon, Alsace); 18 isolates were collected from a single plot (Aquitaine vineyard). Significant linkage disequilibrium indicated that P. chlamydospora populations are not panmictic, whereas the level of haplotypic diversity observed, 72 single multilocus haplotypes identified in total among the 74 isolates analysed, suggest that reproduction in this species may not be strictly clonal. Clustering analyses suggests the presence of two genetically differentiated but sympatric clusters of isolates. The level of differentiation between the two clusters is high (F ST =0.23) and significant at 13 out of the 21 loci analyzed. The most plausible explanation for this pattern of admixture is the coexistence in P. chlamydospora French populations of two predominant clonal lineages. Finally, the low level of spatial genetic differentiation in this study is consistent with the spread of this fungus through the transport of infected plant material by human activities.