Abstract

The oomycetes are a class of microscopic, filamentous eukaryotes within the Stramenopiles-Alveolata-Rhizaria (SAR) supergroup which includes ecologically significant animal and plant pathogens, most infamously the causative agent of potato blight Phytophthora infestans. Single-gene and concatenated phylogenetic studies both of individual oomycete genera and of members of the larger class have resulted in conflicting conclusions concerning species phylogenies within the oomycetes, particularly for the large Phytophthora genus. Genome-scale phylogenetic studies have successfully resolved many eukaryotic relationships by using supertree methods, which combine large numbers of potentially disparate trees to determine evolutionary relationships that cannot be inferred from individual phylogenies alone. With a sufficient amount of genomic data now available, we have undertaken the first whole-genome phylogenetic analysis of the oomycetes using data from 37 oomycete species and 6 SAR species. In our analysis, we used established supertree methods to generate phylogenies from 8,355 homologous oomycete and SAR gene families and have complemented those analyses with both phylogenomic network and concatenated supermatrix analyses. Our results show that a genome-scale approach to oomycete phylogeny resolves oomycete classes and individual clades within the problematic Phytophthora genus. Support for the resolution of the inferred relationships between individual Phytophthora clades varies depending on the methodology used. Our analysis represents an important first step in large-scale phylogenomic analysis of the oomycetes. IMPORTANCE The oomycetes are a class of eukaryotes and include ecologically significant animal and plant pathogens. Single-gene and multigene phylogenetic studies of individual oomycete genera and of members of the larger classes have resulted in conflicting conclusions concerning interspecies relationships among these species, particularly for the Phytophthora genus. The onset of next-generation sequencing techniques now means that a wealth of oomycete genomic data is available. For the first time, we have used genome-scale phylogenetic methods to resolve oomycete phylogenetic relationships. We used supertree methods to generate single-gene and multigene species phylogenies. Overall, our supertree analyses utilized phylogenetic data from 8,355 oomycete gene families. We have also complemented our analyses with superalignment phylogenies derived from 131 single-copy ubiquitous gene families. Our results show that a genome-scale approach to oomycete phylogeny resolves oomycete classes and clades. Our analysis represents an important first step in large-scale phylogenomic analysis of the oomycetes.

Highlights

  • The oomycetes are a class of microscopic, filamentous eukaryotes within the Stramenopiles-Alveolata-Rhizaria (SAR) supergroup which includes ecologically significant animal and plant pathogens, most infamously the causative agent of potato blight Phytophthora infestans

  • Initial internal transcribed spacer (ITS) phylogeny data reported by Cooke et al (41) suggested that Phytophthora was paraphyletic with respect to basal clades 9 and 10; later multigene and combined nuclear and mitochondrial studies have placed these clades within Phytophthora (42, 44, 45)

  • We constructed a data set containing 43 complete genomes, consisting of 37 from oomycete species and 6 outgroups from other species within the SAR supergroup (Materials and Methods; Table 1). Of these 37 oomycete genomes, 26 were from either Phytophthora species or Pythium species representing the majority of clades within both genera, and the remainder were sampled from all four of the “crown” orders (66–89)

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Summary

Introduction

The oomycetes are a class of microscopic, filamentous eukaryotes within the Stramenopiles-Alveolata-Rhizaria (SAR) supergroup which includes ecologically significant animal and plant pathogens, most infamously the causative agent of potato blight Phytophthora infestans. Single-gene and concatenated phylogenetic studies both of individual oomycete genera and of members of the larger class have resulted in conflicting conclusions concerning species phylogenies within the oomycetes, for the large Phytophthora genus. Single-gene and multigene phylogenetic studies of individual oomycete genera and of members of the larger classes have resulted in conflicting conclusions concerning interspecies relationships among these species, for the Phytophthora genus. Phytophthora is the largest genus (Ͼ120 described species) within the order Peronosporales and was divided into 10 phylogenetic clades on the basis of initial internal transcribed spacer (ITS) analysis and, later, combined nuclear and mitochondrial analyses (41, 42) (Fig. 2a). Blair et al (42) found strong support by maximum-likelihood, maximum-parsimony, and Bayesian methods for the 10 phylogenetic clades using data from seven highly conserved nuclear loci (including markers from 28S ribosomal DNA [rDNA], Hsp, and ␤-tubulin) msphere.asm.org 2

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