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Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation.

ABSTRACT: BACKGROUND:Oomycetes are a group of filamentous eukaryotic microorganisms that have colonized all terrestrial and oceanic ecosystems, and they include prominent plant pathogens. The Aphanomyces genus is unique in its ability to infect both plant and animal species, and as such exemplifies oomycete versatility in adapting to different hosts and environments. Dissecting the underpinnings of oomycete diversity provides insights into their specificity and pathogenic mechanisms. RESULTS:By carrying out genomic analyses of the plant pathogen A. euteiches and the crustacean pathogen A. astaci, we show that host specialization is correlated with specialized secretomes that are adapted to the deconstruction of the plant cell wall in A. euteiches and protein degradation in A. astaci. The A. euteiches genome is characterized by a large repertoire of small secreted protein (SSP)-encoding genes that are highly induced during plant infection, and are not detected in other oomycetes. Functional analysis revealed an SSP from A. euteiches containing a predicted nuclear-localization signal which shuttles to the plant nucleus and increases plant susceptibility to infection. CONCLUSION:Collectively, our results show that Aphanomyces host adaptation is associated with evolution of specialized secretomes and identify SSPs as a new class of putative oomycete effectors.

SUBMITTER: Gaulin E

PROVIDER: S-EPMC5907361 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation.

Gaulin Elodie E Pel Michiel J C MJC Camborde Laurent L San-Clemente Hélène H Courbier Sarah S Dupouy Marie-Alexane MA Lengellé Juliette J Veyssiere Marine M Le Ru Aurélie A Grandjean Frédéric F Cordaux Richard R Moumen Bouziane B Gilbert Clément C Cano Liliana M LM Aury Jean-Marc JM Guy Julie J Wincker Patrick P Bouchez Olivier O Klopp Christophe C Dumas Bernard B

BMC biology 20180418 1

<h4>Background</h4>Oomycetes are a group of filamentous eukaryotic microorganisms that have colonized all terrestrial and oceanic ecosystems, and they include prominent plant pathogens. The Aphanomyces genus is unique in its ability to infect both plant and animal species, and as such exemplifies oomycete versatility in adapting to different hosts and environments. Dissecting the underpinnings of oomycete diversity provides insights into their specificity and pathogenic mechanisms.<h4>Results</h ...[more]

PMID: 29669603

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Project description:BackgroundAphanomyces root rot is one of the most severe diseases in sugar beet (Beta vulgaris L.), resulting in drastic losses in sugar yield and plant degeneration. The causal agent is the soil-borne pathogen Aphanomyces cochlioides, a phytopathogenic oomycete able to infect sugar beet roots from the seedling stage until harvest. Reliable control measures and fully resistant varieties to prevent the disease on mature roots are currently not available. Furthermore, the quantitative nature of the resistance mechanisms to the root rot disease remain unclear. With the aim to identify key genes involved in plant defense responses against the root rot, we performed a transcriptome analysis of sugar beet interactions with A. cochlioides. The transcriptome responses of two partially resistant and two susceptible sugar beet breeding lines, inoculated with three A. cochlioides isolates with different geographical origins have been investigated in this study.ResultsThe results showed that the transcriptional responses to A. cochlioides infection were mainly genotype-dependent. Comparisons of transcriptome profiles of partially resistant and susceptible breeding lines revealed the presence of differentially expressed genes that play a key role in defense mechanisms during the initial stages of infection. Gene Ontology (GO) categories associated with hydrogen peroxide (H2O2) metabolism, detoxification and cell wall organization were significantly enriched in the differentially expressed gene set from the two partially resistant lines, while photosynthesis-related GO terms were significantly enriched in the two susceptible lines. Unique and overlapping GO categories were over-represented in specific genotype-isolate-time point interactions, indicating that different genotypes respond with common defense strategies as well as specialized responses to different isolates and time points. Transcription factors belonging to the WRKY and ERF families were up-regulated in all genotypes. Furthermore, increased expression of genes encoding for disease resistant proteins have been identified in the two partially resistant genotypes.ConclusionsThis research offers new insights into the transcriptomic events that regulate the sugar beet defense responses to A. cochlioides infection. The findings of this study emphasize the importance of genotype-specific interactions in response to different A. cochlioides isolates. Moreover, the results showed the up-regulation of genes that may play important roles in the defense responses to A. cochlioides which can be used to improve future breeding and to assist in the development of resistant cultivars.

Dataset Information

Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation.

Publications

Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation.

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