Phylogenetic and experimental evidence for host‐specialized cryptic species in a biotrophic oomycete

Abstract

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.

Cryptic Species: A Leitmotif of Contemporary Mycology Has Challenges and Benefits for Plant Pathologists

“…riparia. Each has distinct to partially overlapping host ranges in Vitis and Parthenocissus, both members of the family Vitaceae (Rouxel et al 2013). Although naming the taxa as formae speciales, the authors explicitly refer to them as cryptic species and demonstrate phylogenetic separation on the basis of multiple gene topologies.…”

“…The formae speciales of Rouxel et al (2013) are "clades" in Rouxel et al (2014). Novel taxon P. viticola clade vulpina is restricted to Vitis vulpina, fox grape (Rouxel et al 2014).…”

“…Novel taxon P. viticola clade vulpina is restricted to Vitis vulpina, fox grape (Rouxel et al 2014). Rouxel et al (2013) discuss implications, including breeding for resistance, the importance of understanding spatiotemporal distributions of these cryptic species, and accurate identification.…”

“…Plasmopara viticola, the pseudofungal agent of grape downy mildew, is one of the most important diseases of grape worldwide (Gessler et al 2011). Recent advances have demonstrated that this taxon is composed of multiple cryptic species, each indicated in Rouxel et al (2013) as a forma specialis: Plasmopara viticola f. sp. quinquefolia, f. sp.…”

“…Although naming the taxa as formae speciales, the authors explicitly refer to them as cryptic species and demonstrate phylogenetic separation on the basis of multiple gene topologies. "Some previous research on P. viticola will need to be revisited, because it was unclear which species were under study" (Rouxel et al 2013).…”