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

• Published in: The New phytologist Vol. 197; no. 1; pp. 251 - 263
• Main Authors: Rouxel, Mélanie, Mestre, Pere, Comont, Gwenaelle, Lehman, Brian L., Schilder, Annemiek, Delmotte, François
• Format: Journal Article
• Language: English
• Published: England New Phytologist Trust 01-01-2013; Wiley Subscription Services, Inc; Wiley
• Subjects: Adaptation, Biological; Airborne microorganisms; Alleles; Animal behavior; Assortative mating; Biological taxonomies; Breeding; Butterflies & moths; Crops, Agricultural - microbiology; Cryptic species; Cultivation; disease emergence; Disease resistance; Divergence; DNA, Fungal - genetics; DNA, Ribosomal Spacer - genetics; Downy mildew; Ecosystem; evolution of aggressiveness in agro‐ecosystem; Evolution, Molecular; Fruit cultivation; Genome, Fungal; host plant specialization; Host plants; Host range; host shift; Host Specificity; Inoculation; Life Sciences; Mildews; Morphology; North America; Oomycetes; Oomycetes - classification; Oomycetes - genetics; Oomycetes - pathogenicity; Oomycetes - physiology; Parasite hosts; Parthenocissus quinquefolia; Pathogenicity; Pathogens; Phylogenetics; Phylogeny; Plant Diseases - microbiology; Plant Leaves - microbiology; Plants; plant–pathogen interaction; Plasmopara viticola; Plasmopara viticola (the causal agent of grapevine downy mildew); quantitative adaptation to cultivar; Range extension; Reproductive behaviour; Riparian environments; Specialization; Speciation; Species; Species Specificity; Sporangia; Sporangia - genetics; Sporangia - physiology; Statistics, Nonparametric; Vegetal Biology; Vitaceae; Viticulture; Vitis - microbiology; Vitis aestivalis; Vitis labrusca; Vitis riparia; Vitis vinifera; Vitis vinifera and wild relatives; North America; quantitative adaptation to cultivar; Plasmopara viticola (the causal agent of grapevine downy mildew); host shift; Vitis vinifera and wild relatives; plant–pathogen interaction; disease emergence; evolution of aggressiveness in agro-ecosystem; host plant specialization
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.12016

Assortative 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.