Comparative genomics reveals insight into virulence strategies of plant pathogenic oomycetes.

Bishwo N Adhikari,C Robin Buell,Marcelo M Zerillo,Boris Alexander Vinatzer,John P Hamilton,C André Lévesque,Ned Tisserat

doi:10.1371/journal.pone.0075072

Abstract

The kingdom Stramenopile includes diatoms, brown algae, and oomycetes. Plant pathogenic oomycetes, including Phytophthora, Pythium and downy mildew species, cause devastating diseases on a wide range of host species and have a significant impact on agriculture. Here, we report comparative analyses on the genomes of thirteen straminipilous species, including eleven plant pathogenic oomycetes, to explore common features linked to their pathogenic lifestyle. We report the sequencing, assembly, and annotation of six Pythium genomes and comparison with other stramenopiles including photosynthetic diatoms, and other plant pathogenic oomycetes such as Phytophthora species, Hyaloperonospora arabidopsidis, and Pythium ultimum var. ultimum. Novel features of the oomycete genomes include an expansion of genes encoding secreted effectors and plant cell wall degrading enzymes in Phytophthora species and an over-representation of genes involved in proteolytic degradation and signal transduction in Pythium species. A complete lack of classical RxLR effectors was observed in the seven surveyed Pythium genomes along with an overall reduction of pathogenesis-related gene families in H. arabidopsidis. Comparative analyses revealed fewer genes encoding enzymes involved in carbohydrate metabolism in Pythium species and H. arabidopsidis as compared to Phytophthora species, suggesting variation in virulence mechanisms within plant pathogenic oomycete species. Shared features between the oomycetes and diatoms revealed common mechanisms of intracellular signaling and transportation. Our analyses demonstrate the value of comparative genome analyses for exploring the evolution of pathogenesis and survival mechanisms in the oomycetes. The comparative analyses of seven Pythium species with the closely related oomycetes, Phytophthora species and H. arabidopsidis, and distantly related diatoms provide insight into genes that underlie virulence.

Highlights

Oomycetes are a diverse group of organisms that morphologically resemble Fungi, yet are members of the Straminipila ( = stramenopile) and are more closely related to organisms in aquatic environments such as brown algae and diatoms
Genome Sequencing, Assembly, and Annotation The sequences of six Pythium genomes (Py. aphanidermatum (DAOM BR444 = CBS 132490), Py. arrhenomanes (ATCC 12531 = CBS 324.62), Py. irregulare (DAOM BR486 = CBS 250.28), Py. iwayamai (DAOM 242034 = CBS 132417), Py. ultimum var. sporangiiferum (DAOM BR650 = CBS 219.65), and Py. vexans (DAOM BR484 = CBS 119.80); Table 1) that provide a broad representation of the genus Pythium (Figure 1) were generated using pyrosequencing with the Roche 454 or the Illumina Genome Analyzer (GA) II sequencing-by-synthesis platform
For the five Pythium species (Py. arrhenomanes, Py. irregulare, Py. iwayamai, Py. ultimum var. sporangiiferum, and Py. vexans), 6.6 to 14.4 Gb of purityfiltered (PF) reads were generated by the Illumina GAII/IIx sequencer (Table S1) while for Py. aphanidermatum, 507 Mb of single-end and 137.5 Mb of paired-end reads were generated using pyrosequencing

Summary

Introduction

Oomycetes are a diverse group of organisms that morphologically resemble Fungi, yet are members of the Straminipila ( = stramenopile) and are more closely related to organisms in aquatic environments such as brown algae and diatoms. There has been continuous debate on the existence of chromalveolate hypothesis and the photosynthetic origin of the stramenopiles [8]. The oomycetes include a diverse range of free-living water molds and pathogens of plants, mammals, insects, fish, crustaceans, algae, and various microbes, including fungi [9,10,11,12,13]. Some of the most damaging oomycete genera are Aphanomyces [18], Peronospora [19], Phytophthora [20], Plasmopara [21], Pseudoperonospora [22], and Pythium [23] species; the wide host range of these genera, coupled with the diversity of diseases they cause, pose a challenge to the development of durable disease control strategies in plants

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Conclusion