Transcriptome analysis of enriched Golovinomyces orontii haustoria by deep 454 pyrosequencing

Weßling, Ralf; Schmidt, Sarah M.; Micali, Cristina; Knaust, Florian; Reinhardt, Richard; Neumann, Ulla; Themaat, Emiel Ver Loren van; Panstruga, Ralph

doi:10.1016/j.fgb.2012.04.001

Cited by 44 publications

(58 citation statements)

References 60 publications

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“…Using several criteria including a size cut-off, presence of an N-terminal secretion signal and, due to the rapidly evolving nature of effectors, a lack of homology outside the powdery mildew fungi, we predicted 103 OECs de novo from a sequenced haustorial Gor cDNA library (Weßling et al, 2012). This set of OECs, and candidate effector sequences from the barley powdery mildew Blumeria graminis f. sp.…”

Section: Resultsmentioning

confidence: 99%

“…This set of OECs, and candidate effector sequences from the barley powdery mildew Blumeria graminis f. sp. hordei ( Bgh ), were then used as templates for iterative homology searches in the same haustorial cDNA library (Pedersen et al, 2012; Weßling et al, 2012). These iterations identified two and ten additional OECs, respectively, yielding a total of 115 OECs.…”

Section: Resultsmentioning

confidence: 99%

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Convergent Targeting of a Common Host Protein-Network by Pathogen Effectors from Three Kingdoms of Life

Weßling

Epple

Altmann

et al. 2014

Cell Host & Microbe

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SUMMARY While conceptual principles governing plant immunity are becoming clear, its systems-level organization and the evolutionary dynamic of the host-pathogen interface are still obscure. We generated a systematic protein-protein interaction network of virulence effectors from the ascomycete pathogen Golovinomyces orontii and Arabidopsis thaliana host proteins. We combined this dataset with corresponding data for the eubacterial pathogen Pseudomonas syringae and the oomycete pathogen Hyaloperonospora arabidopsidis. The resulting network identifies host proteins onto which intraspecies and interspecies pathogen effectors converge. Phenotyping of 124 Arabidopsis effector-interactor mutants revealed a correlation between intra- and interspecies convergence and several altered immune response phenotypes. The effectors and most heavily targeted host protein co-localized in sub-nuclear foci. Products of adaptively selected Arabidopsis genes are enriched for interactions with effector targets. Our data suggest the existence of a molecular host-pathogen interface that is conserved across Arabidopsis accessions, while evolutionary adaptation occurs in the immediate network neighborhood of effector targets.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Convergent Targeting of a Common Host Protein-Network by Pathogen Effectors from Three Kingdoms of Life

Weßling

Epple

Altmann

et al. 2014

Cell Host & Microbe

Self Cite

357

437

View full text Add to dashboard Cite

show abstract

“…iab.keio.ac.jp/cgi-bin/NLS_Mapper_form.cgi; Kosugi et al, 2009). Although ADF4 was not identified as an interactor with OECs by Weßling et al (2014), the OECs used in their analysis were identified from a complementary DNA (cDNA) library generated from isolated haustoria and chosen for their possession of canonical secretion peptides (Weßling et al, 2012(Weßling et al, , 2014). In contrast, the Bgh effectors AVR a10 and AVR k1 do not have canonical secretion peptides, although their functionality in the host cytoplasm has been demonstrated (Ridout et al, 2006;Shen et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

2016

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Actin-depolymerizing factors (ADFs) are conserved proteins that function in regulating the structure and dynamics of actin microfilaments in eukaryotes. In this study, we present evidence that Arabidopsis (Arabidopsis thaliana) subclass I ADFs, particularly ADF4, functions as a susceptibility factor for an adapted powdery mildew fungus. The null mutant of ADF4 significantly increased resistance against the adapted powdery mildew fungus Golovinomyces orontii. The degree of resistance was further enhanced in transgenic plants in which the expression of all subclass I ADFs (i.e. ADF1-ADF4) was suppressed. Microscopic observations revealed that the enhanced resistance of adf4 and ADF1-4 knockdown plants (ADF1-4Ri) was associated with the accumulation of hydrogen peroxide and cell death specific to G. orontii-infected cells. The increased resistance and accumulation of hydrogen peroxide in ADF1-4Ri were suppressed by the introduction of mutations in the salicylic acid-and jasmonic acid-signaling pathways but not by a mutation in the ethylene-signaling pathway. Quantification by microscopic images detected an increase in the level of actin microfilament bundling in ADF1-4Ri but not in adf4 at early G. orontii infection time points. Interestingly, complementation analysis revealed that nuclear localization of ADF4 was crucial for susceptibility to G. orontii. Based on its G. orontii-infected-cell-specific phenotype, we suggest that subclass I ADFs are susceptibility factors that function in a direct interaction between the host plant and the powdery mildew fungus.Powdery mildew is an obligate biotrophic fungal pathogen that infects approximately 10,000 plant species, including crops, vegetables, and ornamental plants, thus causing extensive economic losses worldwide (Takamatsu, 2004). In an effort to understand the plant response to powdery mildew fungal infection and the mechanism of plant-powdery mildew fungus interactions, many mutants of host plants, particularly the model plant Arabidopsis (Arabidopsis thaliana), have been identified and analyzed.Genes for which loss causes increased resistance to a pathogen could encode factors involved in the suppression of plant immunity or susceptibility factors that function in support of the pathogenic infection. Previously identified Arabidopsis genes, the loss of whose expression causes enhanced resistance against adapted powdery mildew fungi, include POWDERY MILDEW RESISTANT1 (PMR1)

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“…Recently, the term "dual RNA-seq" was coined to refer to the use of RNA-seq in transcriptomic analyses in which gene expression changes in both the pathogen and the host are analyzed simultaneously (Westermann et al, 2012). Whereas numerous studies have focused on either the pathogen or the host (Xu et al, 2011;Kunjeti et al, 2012;Petre et al, 2012;Weßling et al, 2012;Garnica et al, 2013;Link et al, 2014), only a few have involved the comprehensive analysis of both organisms (Kawahara et al, 2012;Tierney et al, 2012;Fernandez et al, 2012;Lowe et al, 2014;Yamagishi et al, 2014). Here, we present an in-depth transcriptomic analysis of the M. perniciosa-cacao interaction, which vastly expands our current knowledge of WBD and also contributes to our general understanding of plant-pathogen interactions.…”

Section: Discussionmentioning

confidence: 99%

High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction betweenTheobroma cacaoand the Fungal PathogenMoniliophthora perniciosa

et al. 2014

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Witches' broom disease (WBD), caused by the hemibiotrophic fungus Moniliophthora perniciosa, is one of the most devastating diseases of Theobroma cacao, the chocolate tree. In contrast to other hemibiotrophic interactions, the WBD biotrophic stage lasts for months and is responsible for the most distinctive symptoms of the disease, which comprise drastic morphological changes in the infected shoots. Here, we used the dual RNA-seq approach to simultaneously assess the transcriptomes of cacao and M. perniciosa during their peculiar biotrophic interaction. Infection with M. perniciosa triggers massive metabolic reprogramming in the diseased tissues. Although apparently vigorous, the infected shoots are energetically expensive structures characterized by the induction of ineffective defense responses and by a clear carbon deprivation signature. Remarkably, the infection culminates in the establishment of a senescence process in the host, which signals the end of the WBD biotrophic stage. We analyzed the pathogen's transcriptome in unprecedented detail and thereby characterized the fungal nutritional and infection strategies during WBD and identified putative virulence effectors. Interestingly, M. perniciosa biotrophic mycelia develop as long-term parasites that orchestrate changes in plant metabolism to increase the availability of soluble nutrients before plant death. Collectively, our results provide unique insight into an intriguing tropical disease and advance our understanding of the development of (hemi)biotrophic plant-pathogen interactions.

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Transcriptome analysis of enriched Golovinomyces orontii haustoria by deep 454 pyrosequencing

Cited by 44 publications

References 60 publications

Convergent Targeting of a Common Host Protein-Network by Pathogen Effectors from Three Kingdoms of Life

Convergent Targeting of a Common Host Protein-Network by Pathogen Effectors from Three Kingdoms of Life

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

High-Resolution Transcript Profiling of the Atypical Biotrophic Interaction betweenTheobroma cacaoand the Fungal PathogenMoniliophthora perniciosa

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