The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection.

Cindy Martens,Yves Van De Peer

doi:10.1186/1471-2164-11-353

Cindy Martens, Yves Van De Peer

Open Access

https://doi.org/10.1186/1471-2164-11-353

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Abstract

BackgroundOomycetes of the genus Phytophthora are pathogens that infect a wide range of plant species. For dicot hosts such as tomato, potato and soybean, Phytophthora is even the most important pathogen. Previous analyses of Phytophthora genomes uncovered many genes, large gene families and large genome sizes that can partially be explained by significant repeat expansion patterns.ResultsAnalysis of the complete genomes of three different Phytophthora species, using a newly developed approach, unveiled a large number of small duplicated blocks, mainly consisting of two or three consecutive genes. Further analysis of these duplicated genes and comparison with the known gene and genome duplication history of ten other eukaryotes including parasites, algae, plants, fungi, vertebrates and invertebrates, suggests that the ancestor of P. infestans, P. sojae and P. ramorum most likely underwent a whole genome duplication (WGD). Genes that have survived in duplicate are mainly genes that are known to be preferentially retained following WGDs, but also genes important for pathogenicity and infection of the different hosts seem to have been retained in excess. As a result, the WGD might have contributed to the evolutionary and pathogenic success of Phytophthora.ConclusionsThe fact that we find many small blocks of duplicated genes indicates that the genomes of Phytophthora species have been heavily rearranged following the WGD. Most likely, the high repeat content in these genomes have played an important role in this rearrangement process. As a consequence, the paucity of retained larger duplicated blocks has greatly complicated previous attempts to detect remnants of a large-scale duplication event in Phytophthora. However, as we show here, our newly developed strategy to identify very small duplicated blocks might be a useful approach to uncover ancient polyploidy events, in particular for heavily rearranged genomes.

Highlights

Oomycetes of the genus Phytophthora are pathogens that infect a wide range of plant species
P. sojae and P. ramorum have a genome size of 95 Mb and 65 Mb, respectively [12]
The larger size of the P. sojae genome compared to P. ramorum is because of the higher number of predicted genes (16.988 and 14.451, respectively [13]) and because of larger intergenic regions and different retrotransposon expansion patterns [12,15]

Summary

Introduction

Oomycetes of the genus Phytophthora are pathogens that infect a wide range of plant species. Phytophthora infestans, responsible for severe damage in the food production worldwide by infecting tomato and potato [8], was the infective agent of the so-called potato blight that caused the Irish famine between 1845 and 1849, during which approximately one million people died and another million emigrated [9,10] Another species, P. sojae, causes root and stem rot in soybean resulting in huge annual production losses [11]. The larger size of the P. sojae genome compared to P. ramorum is because of the higher number of predicted genes (16.988 and 14.451, respectively [13]) and because of larger intergenic regions and different retrotransposon expansion patterns [12,15]. Comparison of the three Phytophthora genomes revealed an unusual genome organization; i.e. regions with conserved gene order, high gene density and lower repeat content are separated by regions with non-conserved gene order, low gene density and high repeat content [13]

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