Multiple origins of downy mildews and mito-nuclear discordance within the paraphyletic genus Phytophthora

Abstract

Phylogenetic relationships between thirteen species of downy mildew and 103 species of Phytophthora (plant-pathogenic oomycetes) were investigated with two nuclear and four mitochondrial loci, using several likelihood-based approaches. Three Phytophthora taxa and all downy mildew taxa were excluded from the previously recognized subgeneric clades of Phytophthora, though all were strongly supported within the paraphyletic genus. Downy mildews appear to be polyphyletic, with graminicolous downy mildews (GDM), brassicolous downy mildews (BDM) and downy mildews with colored conidia (DMCC) forming a clade with the previously unplaced Phytophthora taxon totara; downy mildews with pyriform haustoria (DMPH) were placed in their own clade with affinities to the obligate biotrophic P. cyperi. Results suggest the recognition of four additional clades within Phytophthora, but few relationships between clades could be resolved. Trees containing all twenty extant downy mildew genera were produced by adding partial coverage of seventeen additional downy mildew taxa; these trees supported the monophyly of the BDMs, DMCCs and DMPHs but suggested that the GDMs are paraphyletic in respect to the BDMs or polyphyletic. Incongruence between nuclear-only and mitochondrial-only trees suggests introgression may have occurred between several clades, particularly those containing biotrophs, questioning whether obligate biotrophic parasitism and other traits with polyphyletic distributions arose independently or were horizontally transferred. Phylogenetic approaches may be limited in their ability to resolve some of the complex relationships between the “subgeneric” clades of Phytophthora, which include twenty downy mildew genera and hundreds of species.

A high-quality grapevine downy mildew genome assembly reveals rapidly evolving and lineage-specific putative host adaptation genes

“…arabidopsidis) were paraphyletic and, consequently, that obligate biotrophy had evolved independently at least twice within this order ( Figure 2B, Supplementary figure 3). These results confirmed other recent phylogenetic analyses (McCarthy & Fitzpatrick 2017;Sharma et al 2015;Bourret et al 2018) contradicting earlier evidence suggesting that downy mildews are monophyletic (Göker et al 2007).…”

Genome reconstruction of the non-culturable spinach downy mildew Peronospora effusa by metagenome filtering

“…Other species within the Peronosporales are the obligate biotrophic downy mildews that cause disease while keeping the plant alive. The relationship between downy mildews and Phytophthora species have long been unresolved [2]. In many studies of oomycete phylogeny, the downy mildew species were barely covered.…”

“…The first phylogenetic trees based on morphological traits and single gene comparisons [3, 4] classified the downy mildews as a sister clade to the Phytophthora species within the order of Peronosporales. Recently, studies using multiple gene and full genome comparisons suggest that the downy mildews have multiple independent origins within the Phytophthora genus [2, 5, 6].…”

A LAMP at the end of the tunnel: a rapid, field deployable assay for the kauri dieback pathogen,Phytophthora agathidicida

“…To identify potential targets for genetic testing, publically available Phytophthora and Pythium mitochondrial genome sequences were obtained from the NCBI RefSeq database [7]. This sample included all five Phytophthora species reported from kauri forests [1,3], all currently recognized representatives of Phytophthora clade 5 [8], and two accessions of P. agathidicida [8].…”

“…Broad phylogenies for the Peronosporaceae (e.g., 4-7) have identified strongly supported sub-clades. For example, Bourret et al [7] described total of 16 sub-clades, the majority of which contain at least one Phytophthora species. The phylogenetic analysis of Weir et al [8] placed P. agathidicida, along with three other formally recognized species, within Clade 5.…”