Article

Mechanisms and Evolution of Virulence in Oomycetes

The Broad Institute of the Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts 02142, USA.
Annual Review of Phytopathology (Impact Factor: 9.62). 09/2012; 50(1):295-318. DOI: 10.1146/annurev-phyto-081211-172912
Source: PubMed

ABSTRACT

Many destructive diseases of plants and animals are caused by oomycetes, a group of eukaryotic pathogens important to agricultural, ornamental, and natural ecosystems. Understanding the mechanisms underlying oomycete virulence and the genomic processes by which those mechanisms rapidly evolve is essential to developing effective long-term control measures for oomycete diseases. Several common mechanisms underlying oomycete virulence, including protein toxins and cell-entering effectors, have emerged from comparing oomycetes with different genome characteristics, parasitic lifestyles, and host ranges. Oomycete genomes display a strongly bipartite organization in which conserved housekeeping genes are concentrated in syntenic gene-rich blocks, whereas virulence genes are dispersed into highly dynamic, repeat-rich regions. There is also evidence that key virulence genes have been acquired by horizontal transfer from other eukaryotic and prokaryotic species.

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    • "reducedcomparedtonumbersofsimilargenesintheirPhytoph- thorahemibiotrophicancestors[10] [39] [66].JiangandTyler[12]have speculatedthatthismaybeanadaptationforstealthbythebiotrophicpathogenspecies ,byreducingthehydrolyticreleaseof carbohydratefragmentsthatmaytriggerPTI. Phytophthorapathogenstypicallyhavelargegenefamilies (40e80copies)encodingnecrosisandethylene-inducingpeptide- likeproteins(NLPs)thatcantriggerplantcelldeath[8] [9]andthese proteinsarethoughttoplayakeyroleinthenecrotrophicphaseof theirlifestyle.However,asmallnumberofNLPshavebeenretained bythedownymildews(Table4),suggestingthatNLPsinobligate biotrophsmayhaverolesinpathogenicityotherthantriggeringcell death[12]. "
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    ABSTRACT: Plasmopara viticola is an oomycete pathogen that causes downy mildew, one of the most devastating diseases of grapevine. Currently, the molecular basis of the interaction between this pathogen and the grapevine host is not well understood. To explore the genes involved in P. viticola pathogenicity we performed RNA-Seq analysis of cDNAs derived from downy mildew-infected grapevine leaves for three different P. viticola isolates; two from China (JL-7-2, ZJ-1-1) and one from Australia (CSIRO-L-2). Approximately 30,000 unigenes were predicted for each of the three isolates and from these over 500 potential secreted proteins were identified. Using three prediction methods, a total of 51 PvRXLR effectors were identified to be present in the secretome, with at least 26 shared by two or more P. viticola isolates. Expression profiling, based on RNA-Seq data, indicated that PvRXLRs showed three different expression patterns during infection. Transient expression of selected PvRXLRs in Nicotiana benthamiana demonstrated that all were capable of suppressing programmed cell death triggered by the mouse BAX protein or the PAMP INF1. Additionally, BLASTP and Hidden Markov Model (HMM) searches identified 10 predicted proteins belonging to the CRN (Crinkler) group of oomycete effectors. Pfam domain analysis of the secretome also identified a diverse range of putative apoplastic effectors, the major groups being glycosyl hydrolases, peptidases and protease-inhibitors. This study provides the first detailed analysis of the secretome of grapevine downy mildew and its encoded effector arsenal.
    Full-text · Article · Jul 2015 · Physiological and Molecular Plant Pathology
    • "While they morphologically resemble fungi, oomycetes are taxonomically more closely related to brown algae, diatoms, and Labyrinthulomycota with which they form the Heterokontobionta (Bartnicki-Garcia 1968; Thines 2014; Spring 2012). Worldwide, plant-pathogenic oomycetes cause some of the most devastating diseases of crops, ornamentals, and native species, leading to yield loss and damage to agricultural and natural ecosystems (Jiang and Tyler 2012). Some of the most destructive oomycete pathogens occur within the order Peronosporales. "
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    ABSTRACT: Downy mildews are oomycete pathogens that cause diseases on a wide range of plant species. Individual species have narrow host ranges and exhibit high degrees of host specialization. Their obligate biotrophic nature makes their study challenging compared to culturable oomycetes, such as Phytophthora spp. and Pythium spp. Next generation sequencing technologies offer unprecedented opportunities for comparative genome-wide analyses of large numbers of isolates rapidly and at low cost. We are utilizing these new technologies to efficiently generate genome assemblies and to study the evolutionary relationships and the effector repertoires within and between diverse species of downy mildew. These include geographically and temporally separated isolates of lettuce downy mildew (Bremia lactucae), tobacco downy mildew (Peronospora tabacina), sorghum and maize downy mildew (Peronosclerospora sorghi), and pearl millet downy mildew (Sclerospora graminicola). We have assembled and annotated these genomes and examined variations in genome size, repeat content, gene content, level of heterozygosity, and the repertoires of genes encoding effectors and other pathogenicity-related proteins, as well as their mitochondrial structure and variation. These downy mildew species differ greatly in genome size and possess varying levels of heterozygosity, indicative of inbreeding, clonal, and outbreeding mating systems. Effector repertoires are diverse between isolates of the same species and between species; many effector-encoding genes appear to be species specific. Our workflow for comparative population genomics and genome analysis are also applicable to rust pathogens.
    No preview · Conference Paper · Jul 2015
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    • "While they morphologically resemble fungi, oomycetes are taxonomically more closely related to brown algae, diatoms, and Labyrinthulomycota with which they form the Heterokontobionta (Bartnicki-Garcia 1968; Thines 2014; Spring 2012). Worldwide, plant-pathogenic oomycetes cause some of the most devastating diseases of crops, ornamentals, and native species, leading to yield loss and damage to agricultural and natural ecosystems (Jiang and Tyler 2012). Some of the most destructive oomycete pathogens occur within the order Peronosporales. "
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    ABSTRACT: Peronospora tabacina is an obligate biotrophic oomycete that causes blue mold or downy mildew on tobacco (Nicotiana tabacum). It is an economically important disease occurring frequently in tobacco growing regions worldwide. We have sequenced and characterized the genomes of two P. tabacina isolates and mined them for pathogenicity related proteins and effector encoding genes. De novo assembly of the genomes using Illumina reads resulted in 4,016 (63.1 Mb, N50 = 79 kb) and 3,245 (55.3 Mb, N50 = 61 kb) scaffolds for isolates 968-J2 and 968-S26 respectively, with an estimated genome size of 68 Mb. The mitochondrial genome has a similar size (~43 kb) and structure to those of other oomycetes, plus several minor unique features. Repetitive elements, primarily retrotransposons, make up ~24% of the nuclear genome. Approximately 18 K protein coding gene models were predicted. Mining the secretome revealed ~120 candidate RxLR, ~6 CRN and ~61 WY-domain containing proteins. Candidate RxLR effectors were shown to be predominantly undergoing diversifying selection, with ~57% located in variable gene-sparse regions of the genome. Aligning the P. tabacina genome to Hyaloperonospora arabidopsidis and Phytophthora spp. revealed a high level of synteny. Blocks of synteny show gene inversions and instances of expansion in intergenic regions. Extensive rearrangements of the gene-rich genomic regions do not appear to have occurred during the evolution of these highly variable pathogens. These assemblies provide the basis for studies of virulence in this and other downy mildew pathogens.
    Full-text · Article · Jul 2015 · Molecular Plant-Microbe Interactions
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