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Identification and Characterization of Nep1-Like Proteins From the Grapevine Downy Mildew Pathogen Plasmopara viticola.

ABSTRACT: The obligate biotrophic oomycete Plasmopara viticola causes tremendous problems in viticulture by evoking grapevine downy mildew. P. viticola, like other plant pathogens, achieves infection by suppression of plant innate immunity by secretion of effector molecules into its host plant. An ever-expanding family of proteins with effector-like characteristics is formed by the "Necrosis and Ethylene inducing peptide 1 (Nep1)-like proteins" (NLPs). NLPs can be divided into two groups by their ability to induce necrosis. While cytotoxic NLPs may act as virulence factors for a necrotrophic or hemibiotrophic plant pathogen, the role of non-cytotoxic NLPs is so far unknown. In this study, we identified eight independent NLPs in P. viticola and selected three for functional analysis. While one was identified as a putative pseudo gene, two contain all so far described critical key elements for necrosis formation except for an N-terminal signal peptide. Further characterization revealed that none of the putative necrosis elicitors was able to actually induce necrosis, neither in several susceptible or resistant Vitis species nor in the dicot model plant Nicotiana benthamiana. This inability exists independently of the presence or absence of a signal peptide. However, any possible mechanism for the suppression of the ability to induce necrosis in planta was not detected. Interestingly, expression analysis of the presumed pseudo gene revealed remarkable differences between pure sporangia solution and sporangia in the presence of leaf material. To our knowledge, this is the first report of this kind of regulation that suggests an important function of so far nonfunctional "pseudo" NLP genes during the first hours of infection.

SUBMITTER: Schumacher S

PROVIDER: S-EPMC7031652 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Identification and Characterization of Nep1-Like Proteins From the Grapevine Downy Mildew Pathogen Plasmopara viticola.

Schumacher Stefan S Grosser Katrin K Voegele Ralf Thomas RT Kassemeyer Hanns-Heinz HH Fuchs René R

Frontiers in plant science 20200213

The obligate biotrophic oomycete Plasmopara viticola causes tremendous problems in viticulture by evoking grapevine downy mildew. P. viticola, like other plant pathogens, achieves infection by suppression of plant innate immunity by secretion of effector molecules into its host plant. An ever-expanding family of proteins with effector-like characteristics is formed by the "Necrosis and Ethylene inducing peptide 1 (Nep1)-like proteins" (NLPs). NLPs can be divided into two groups by ...[more]

PMID: 32117400

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Project description:UNLABELLED:Downy mildew of sunflower is caused by Plasmopara halstedii (Farlow) Berlese & de Toni. Plasmopara halstedii is an obligate biotrophic oomycete pathogen that attacks annual Helianthus species and cultivated sunflower, Helianthus annuus. Depending on the sunflower developmental stage at which infection occurs, the characteristic symptoms range from young seedling death, plant dwarfing, leaf bleaching and sporulation to the production of infertile flowers. Downy mildew attacks can have a great economic impact on sunflower crops, and several Pl resistance genes are present in cultivars to protect them against the disease. Nevertheless, some of these resistances have been overcome by the occurrence of novel isolates of the pathogen showing increased virulence. A better characterization of P.?halstedii infection and dissemination mechanisms, and the identification of the molecular basis of the interaction with sunflower, is a prerequisite to efficiently fight this pathogen. This review summarizes what is currently known about P.?halstedii, provides new insights into its infection cycle on resistant and susceptible sunflower lines using scanning electron and light microscopy imaging, and sheds light on the pathogenicity factors of P.?halstedii obtained from recent molecular data. TAXONOMY:Kingdom Stramenopila; Phylum Oomycota; Class Oomycetes; Order Peronosporales; Family Peronosporaceae; Genus Plasmopara; Species Plasmopara halstedii. DISEASE SYMPTOMS:Sunflower seedling damping off, dwarfing of the plant, bleaching of leaves, starting from veins, and visible white sporulation, initially on the lower side of cotyledons and leaves. Plasmopara halstedii infection may severely impact sunflower seed yield. INFECTION PROCESS:In spring, germination of overwintered sexual oospores leads to sunflower root infection. Intercellular hyphae are responsible for systemic plant colonization and the induction of disease symptoms. Under humid and fresh conditions, dissemination structures are produced by the pathogen on all plant organs to release asexual zoosporangia. These zoosporangia play an important role in pathogen dissemination, as they release motile zoospores that are responsible for leaf infections on neighbouring plants. DISEASE CONTROL:Disease control is obtained by both chemical seed treatment (mefenoxam) and the deployment of dominant major resistance genes, denoted Pl. However, the pathogen has developed fungicide resistance and has overcome some plant resistance genes. Research for more sustainable strategies based on the identification of the molecular basis of the interaction are in progress. USEFUL WEBSITES:http://www.heliagene.org/HP, http://lipm-helianthus.toulouse.inra.fr/dokuwiki/doku.php?id=start, https://www.heliagene.org/PlasmoparaSpecies (soon available).

Project description:BackgroundThe oomycete Plasmopara viticola (Berk. and Curt.) Berl. and de Toni causes downy mildew in grapevine (Vitis vinifera L.). This pathogen is strictly biotrophic, thus completely dependent on living host cells for its survival. The molecular basis of compatibility and disease development in this system is poorly understood. We have carried out a large-scale cDNA-AFLP analysis to identify grapevine and P. viticola genes associated with the infection process.ResultsWe carried out cDNA-AFLP analysis on artificially infected leaves of the susceptible cultivar Riesling at the oil spot stage, on water-treated leaves and on a sample of pure sporangia as controls. Selective amplifications with 128 primer combinations allowed the visualization of about 7000 transcript-derived fragments (TDFs) in infected leaves, 1196 of which (17%) were differentially expressed. We sequenced 984 fragments, 804 of which were identified as grapevine transcripts after homology searching, while 96 were homologous to sequences in Phytophthora spp. databases and were attributed to P. viticola. There were 82 orphan TDFs. Many grapevine genes spanning almost all functional categories were downregulated during infection, especially genes involved in photosynthesis. Grapevine genes homologous to known resistance genes also tended to be repressed, as were several resistance gene analogs and carbonic anhydrase (recently implicated in pathogen resistance). In contrast, genes encoding cytoskeletal components, enzymes of the phenylpropanoid and beta-oxidation pathways, and pathogenesis related proteins were primarily upregulated during infection. The majority of P. viticola transcripts expressed in planta showed homology to genes of unknown function or to genomic Phytophthora sequences, but genes related to metabolism, energy production, transport and signal transduction were also identified.ConclusionThis study provides the first global catalogue of grapevine and P. viticola genes expressed during infection, together with their functional annotations. This will help to elucidate the molecular basis of the infection process and identify genes and chemicals that could help to inhibit the pathogen.

Dataset Information

Identification and Characterization of Nep1-Like Proteins From the Grapevine Downy Mildew Pathogen Plasmopara viticola.

Publications

Identification and Characterization of Nep1-Like Proteins From the Grapevine Downy Mildew Pathogen <i>Plasmopara viticola</i>.

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