scholarly journals Downy Mildew effector HaRxL21 interacts with the transcriptional repressor TOPLESS to promote pathogen susceptibility

2020 ◽  
Author(s):  
Sarah Harvey ◽  
Priyanka Kumari ◽  
Dmitry Lapin ◽  
Thomas Griebel ◽  
Richard Hickman ◽  
...  
Keyword(s):  
Downy Mildew ◽  
Transcriptional Repression ◽  
Plant Immunity ◽  
Effector Proteins ◽  
Host Susceptibility ◽  
Close Relative ◽  
C Terminus ◽  
Rxlr Effector ◽  
Oomycete Pathogen ◽  
Hyaloperonospora Arabidopsidis

AbstractHyaloperonospora arabidopsidis (Hpa) is an oomycete pathogen causing Arabidopsis downy mildew. Effector proteins secreted from the pathogen into the plant play key roles in promoting infection by suppressing plant immunity and manipulating the host to the pathogen’s advantage. One class of oomycete effectors share a conserved ‘RxLR’ motif critical for their translocation into the host cell. Here we characterize the interaction between an RxLR effector, HaRxL21 (RxL21), and the Arabidopsis transcriptional co-repressor Topless (TPL). We establish that RxL21 and TPL interact via an EAR motif at the C-terminus of the effector, mimicking the host plant mechanism for recruiting TPL to sites of transcriptional repression. We show that this motif, and hence interaction with TPL, is necessary for the virulence function of the effector. Furthermore, we provide evidence that RxL21 uses the interaction with TPL, and its close relative TPL-related 1, to repress plant immunity and enhance host susceptibility to both biotrophic and necrotrophic pathogens.

scholarly journals An oomycete RXLR effector triggers antagonistic plant hormone crosstalk to suppress host immunity

2019 ◽  
Author(s):  
Ryan Anderson ◽  
Devdutta Deb ◽  
John Withers ◽  
Sheng Yang He ◽  
John McDowell
Keyword(s):  
Plant Immunity ◽  
Effector Proteins ◽  
Type Iii Effectors ◽  
Hormone Crosstalk ◽  
Regulatory Cascade ◽  
Rxlr Effector ◽  
Plant Pathogen Interactions ◽  
Hyaloperonospora Arabidopsidis ◽  
Cell Networks ◽  
Bacterial Type

ABSTRACTUnderstanding the mechanisms through which pathogens alter plant cell networks is essential for understanding plant-pathogen interactions and will inform efforts to reduce crop diseases. Oomycetes secrete diverse effector proteins into plant cells. The mechanisms through which these effectors promote virulence are largely unknown. We show that the HaRxL10 effector protein from the Arabidopsis thaliana pathogen Hyaloperonospora arabidopsidis (Hpa) targets a transcriptional repressor (JAZ3) involved in jasmonic acid (JA) signalling. This manipulation activates a regulatory cascade that inhibits salicylic acid (SA) signalling, which normally restricts Hpa infection. This virulence mechanism is functionally equivalent to but mechanistically distinct from activation of the antagonistic JA-SA hormone crosstalk by the bacterial JA-mimicking toxin coronatine and by bacterial Type III effectors. These results reveal a key role for JAZ3 in plant immunity and emphasize that JA-SA crosstalk is an Achilles’ heel in the plant immune system, vulnerable to manipulation by diverse microbes.

scholarly journals Multiple Candidate Effectors from the Oomycete Pathogen Hyaloperonospora arabidopsidis Suppress Host Plant Immunity

2011 ◽  
Vol 7 (11) ◽  
pp. e1002348 ◽  
Author(s):  
Georgina Fabro ◽  
Jens Steinbrenner ◽  
Mary Coates ◽  
Naveed Ishaque ◽  
Laura Baxter ◽  
...  
Keyword(s):  
Host Plant ◽  
Plant Immunity ◽  
Oomycete Pathogen ◽  
Hyaloperonospora Arabidopsidis

scholarly journals A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling

2021 ◽  
Vol 17 (3) ◽  
pp. e1009388
Author(s):  
Gan Ai ◽  
Qingyue Xia ◽  
Tianqiao Song ◽  
Tianli Li ◽  
Hai Zhu ◽  
...  
Keyword(s):  
Higher Plants ◽  
Plant Immunity ◽  
Phytophthora Capsici ◽  
Kinase Domain ◽  
Phytophthora Sojae ◽  
Effector Proteins ◽  
Ros Accumulation ◽  
Oomycete Pathogen ◽  
Cellular Defenses

Phytophthora genomes encode a myriad of Crinkler (CRN) effectors, some of which contain putative kinase domains. Little is known about the host targets of these kinase-domain-containing CRNs and their infection-promoting mechanisms. Here, we report the host target and functional mechanism of a conserved kinase CRN effector named CRN78 in a notorious oomycete pathogen, Phytophthora sojae. CRN78 promotes Phytophthora capsici infection in Nicotiana benthamiana and enhances P. sojae virulence on the host plant Glycine max by inhibiting plant H2O2 accumulation and immunity-related gene expression. Further investigation reveals that CRN78 interacts with PIP2-family aquaporin proteins including NbPIP2;2 from N. benthamiana and GmPIP2-13 from soybean on the plant plasma membrane, and membrane localization is necessary for virulence of CRN78. Next, CRN78 promotes phosphorylation of NbPIP2;2 or GmPIP2-13 using its kinase domain in vivo, leading to their subsequent protein degradation in a 26S-dependent pathway. Our data also demonstrates that NbPIP2;2 acts as a H2O2 transporter to positively regulate plant immunity and reactive oxygen species (ROS) accumulation. Phylogenetic analysis suggests that the phosphorylation sites of PIP2 proteins and the kinase domains of CRN78 homologs are highly conserved among higher plants and oomycete pathogens, respectively. Therefore, this study elucidates a conserved and novel pathway used by effector proteins to inhibit host cellular defenses by targeting and hijacking phosphorylation of plant aquaporin proteins.

scholarly journals Disease-Specific Expression of Host Genes During Downy Mildew Infection of Arabidopsis

2009 ◽  
Vol 22 (9) ◽  
pp. 1104-1115 ◽  
Author(s):  
Robin P. Huibers ◽  
Mark de Jong ◽  
René W. Dekter ◽  
Guido Van den Ackerveken
Keyword(s):  
Downy Mildew ◽  
In Silico Analysis ◽  
Effector Proteins ◽  
Ethylene Response Factor ◽  
Promoter Regions ◽  
Specific Expression ◽  
Transcription Factor Genes ◽  
Responsive Element ◽  
Hyaloperonospora Arabidopsidis ◽  
Incompatible Interactions

Here, we report on the identification of Arabidopsis genes that are induced during compatible but not during incompatible interactions with the downy mildew pathogen Hyaloperonospora arabidopsidis. This set of so-called compatible specific (CS) genes contrasts with the large group of defense-associated genes that is differentially expressed during both compatible and incompatible interactions. From the 17 identified CS genes, 6 belong to the ethylene response factor (ERF) family of transcription factor genes, suggesting that these ERF have a role during compatibility. The majority of CS genes are differentially regulated in response to various forms of abiotic stress. In silico analysis of the CS genes revealed an over-representation of dehydration-responsive element/C-repeat binding factor (DREB1A/CBF3) binding sites and EveningElement motifs in their promoter regions. The CS-ERF are closely related to the CBF transcription factors and could potentially bind the DREB1A/CBF3 promoter elements in the CS genes. Transcript levels of CS genes peak at 2 to 3 days postinoculation, when pathogen growth is highest, and decline at later stages of infection. The induction of several CS genes was found to be isolate specific. This suggests that the identified CS genes could be the direct or indirect targets of downy mildew effector proteins that promote disease susceptibility.

scholarly journals The RXLR Effector PcAvh1 Is Required for Full Virulence of Phytophthora capsici

2019 ◽  
Vol 32 (8) ◽  
pp. 986-1000 ◽  
Author(s):  
Xiao-Ren Chen ◽  
Ye Zhang ◽  
Hai-Yang Li ◽  
Zi-Hui Zhang ◽  
Gui-Lin Sheng ◽  
...  
Keyword(s):  
Plant Pathogens ◽  
Plant Immunity ◽  
Phytophthora Capsici ◽  
Ectopic Expression ◽  
Plant Cells ◽  
Effector Proteins ◽  
Bell Pepper ◽  
Broad Host Range ◽  
Virus Induced Gene Silencing ◽  
Rxlr Effector

Plant pathogens employ diverse secreted effector proteins to manipulate host physiology and defense in order to foster diseases. The destructive Phytophthora pathogens encode hundreds of cytoplasmic effectors, which are believed to function inside the plant cells. Many of these cytoplasmic effectors contain the conserved N-terminal RXLR motif. Understanding the virulence function of RXLR effectors will provide important knowledge of Phytophthora pathogenesis. Here, we report the characterization of RXLR effector PcAvh1 from the broad–host range pathogen Phytophthora capsici. Only expressed during infection, PcAvh1 is quickly induced at the early infection stages. CRISPR/Cas9-knockout of PcAvh1 in P. capsici severely impairs virulence while overexpression enhances disease development in Nicotiana benthamiana and bell pepper, demonstrating that PcAvh1 is an essential virulence factor. Ectopic expression of PcAvh1 induces cell death in N. benthamiana, tomato, and bell pepper. Using yeast two-hybrid screening, we found that PcAvh1 interacts with the scaffolding subunit of the protein phosphatase 2A (PP2Aa) in plant cells. Virus-induced gene silencing of PP2Aa in N. benthamiana attenuates resistance to P. capsici and results in dwarfism, suggesting that PP2Aa regulates plant immunity and growth. Collectively, these results suggest that PcAvh1 contributes to P. capsici infection, probably through its interaction with host PP2Aa.

scholarly journals The Phytophthora sojae Avr1d Gene Encodes an RxLR-dEER Effector with Presence and Absence Polymorphisms Among Pathogen Strains

2013 ◽  
Vol 26 (8) ◽  
pp. 958-968 ◽  
Author(s):  
Weixiao Yin ◽  
Suomeng Dong ◽  
Luchong Zhai ◽  
Yachun Lin ◽  
Xiaobo Zheng ◽  
...  
Keyword(s):  
Transient Expression ◽  
Nicotiana Benthamiana ◽  
Plant Immunity ◽  
Phytophthora Sojae ◽  
Transcriptional Analysis ◽  
Mapping Data ◽  
Rxlr Effector ◽  
Effector Triggered Immunity ◽  
Oomycete Pathogen ◽  
Avr Genes

Soybean root and stem rot is caused by the oomycete pathogen Phytophthora sojae. The interaction between P. sojae and soybean fits the “gene-for-gene” hypothesis. Although more than 10 P. sojae avirulence (Avr) effectors have been genetically identified, nearly half of genetically defined avr genes have been cloned. In a previous bioinformatic and global transcriptional analysis, we identified a P. sojae RxLR effector, Avr1d, which was 125 amino acids in length. Mapping data demonstrated that Avr1d presence or absence in the genome was co-segregated with the Avr1d avirulence phenotype in F2 populations. Transient expression of the Avr1d gene using co-bombardment in soybean isogenic lines revealed that this gene triggered a hypersensitive response (HR) in the presence of Rps1d. Sequencing of Avr1d genes in different P. sojae strains revealed two Avr1d alleles. Although polymorphic, the two Avr1d alleles could trigger Rps1d-mediated HR. P. sojae strains carrying either of the alleles were avirulent on Rps1d soybean lines. Avr1d was upregulated during the germinating cyst and early infection stages. Furthermore, transient expression of Avr1d in Nicotiana benthamiana suppressed BAX-induced cell death and enhanced P. capsici infection. Avr1d also suppressed effector-triggered immunity induction by associating with Avr1b and Rps1b, suggestive of a role in suppressing plant immunity.

scholarly journals CRISPR/Cas9-mediated mutagenesis of sweet basil candidate susceptibility gene ObDMR6 enhances downy mildew resistance

PLoS ONE ◽  
2021 ◽  
Vol 16 (6) ◽  
pp. e0253245
Author(s):  
Jeremieh Abram R. Hasley ◽  
Natasha Navet ◽  
Miaoying Tian
Keyword(s):  
Downy Mildew ◽  
Susceptibility Gene ◽  
Downy Mildew Resistance ◽  
Mildew Resistance ◽  
Sweet Basil ◽  
Guide Rnas ◽  
Oomycete Pathogen ◽  
Hyaloperonospora Arabidopsidis ◽  
S Genes ◽  
Downy Mildew Disease

Sweet basil (Ocimum basilicum) is an economically important allotetraploid (2n = 4x = 48) herb whose global production is threatened by downy mildew disease caused by the obligate biotrophic oomycete, Peronospora belbahrii. Generation of disease resistant cultivars by mutagenesis of susceptibility (S) genes via CRISPR/Cas9 is currently one of the most promising strategies to maintain favored traits while improving disease resistance. Previous studies have identified Arabidopsis DMR6 (Downy Mildew Resistance 6) as an S gene required for pathogenesis of the downy mildew-causing oomycete pathogen Hyaloperonospora arabidopsidis. In this study, a sweet basil homolog of DMR6, designated ObDMR6, was identified in the popular sweet basil cultivar Genoveser and found to exist with a high copy number in the genome with polymorphisms among the variants. Two CRISPR/Cas9 constructs expressing one or two single guide RNAs (sgRNAs) targeting the conserved regions of ObDMR6 variants were generated and used to transform Genoveser via Agrobacterium-mediated transformation. 56 T0 lines were generated, and mutations of ObDMR6 were detected by analyzing the Sanger sequencing chromatograms of an ObDMR6 fragment using the Interference of CRISPR Edits (ICE) software. Among 54 lines containing mutations in the targeted sites, 13 had an indel percentage greater than 96% suggesting a near-complete knockout (KO) of ObDMR6. Three representative transgene-free lines with near-complete KO of ObDMR6 determined by ICE were identified in the T1 segregating populations derived from three independent T0 lines. The mutations were further confirmed using amplicon deep sequencing. Disease assays conducted on T2 seedlings of the above T1 lines showed a reduction in production of sporangia by 61–68% compared to the wild-type plants and 69–93% reduction in relative pathogen biomass determined by quantitative PCR (qPCR). This study not only has generated transgene-free sweet basil varieties with improved downy mildew resistance, but also contributed to our understanding of the molecular interactions of sweet basil-P. belbahrii.

scholarly journals 454 Genome Sequencing of Pseudoperonospora cubensis Reveals Effector Proteins with a QXLR Translocation Motif

2011 ◽  
Vol 24 (5) ◽  
pp. 543-553 ◽  
Author(s):  
Miaoying Tian ◽  
Joe Win ◽  
Elizabeth Savory ◽  
Alyssa Burkhardt ◽  
Michael Held ◽  
...  
Keyword(s):  
Genomic Sequence ◽  
Effector Proteins ◽  
Pseudoperonospora Cubensis ◽  
Sequence Information ◽  
Rxlr Effectors ◽  
Rxlr Effector ◽  
Pathogen Fitness ◽  
Oomycete Pathogen ◽  
Bona Fide ◽  
Secreted Peptides

Pseudoperonospora cubensis is a biotrophic oomycete pathogen that causes downy mildew of cucurbits, a devastating foliar disease threatening cucurbit production worldwide. We sequenced P. cubensis genomic DNA using 454 pyrosequencing and obtained random genomic sequences covering approximately 14% of the genome, thus providing the first set of useful genomic sequence information for P. cubensis. Using bioinformatics approaches, we identified 32 putative RXLR effector proteins. Interestingly, we also identified 29 secreted peptides with high similarity to RXLR effectors at the N-terminal translocation domain, yet containing an R-to-Q substitution in the first residue of the translocation motif. Among these, a family of QXLR-containing proteins, designated as PcQNE, was confirmed to have a functional signal peptide and was further characterized as being localized in the plant nucleus. Internalization of secreted PcQNE into plant cells requires the QXLR-EER motif. This family has a large number of near-identical copies within the P. cubensis genome, is under diversifying selection at the C-terminal domain, and is upregulated during infection of plants, all of which are common characteristics of characterized oomycete effectors. Taken together, the data suggest that PcQNE are bona fide effector proteins with a QXLR translocation motif, and QXLR effectors are prevalent in P. cubensis. Furthermore, the massive duplication of PcQNE suggests that they might play pivotal roles in pathogen fitness and pathogenicity.

scholarly journals A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Haiyang Li ◽  
Haonan Wang ◽  
Maofeng Jing ◽  
Jinyi Zhu ◽  
Baodian Guo ◽  
...  
Keyword(s):  
Root Rot ◽  
Plant Immunity ◽  
Phytophthora Sojae ◽  
Host Immunity ◽  
Effector Proteins ◽  
Nuclear Speckles ◽  
Rxlr Effector ◽  
Plant Susceptibility

Oomycete pathogens secrete host cell-entering effector proteins to manipulate host immunity during infection. We previously showed that PsAvh52, an early-induced RxLR effector secreted from the soybean root rot pathogen, Phytophthora sojae, could suppress plant immunity. Here, we found that PsAvh52 is required for full virulence on soybean and binds to a novel soybean transacetylase, GmTAP1, in vivo and in vitro. PsAvh52 could cause GmTAP1 to relocate into the nucleus where GmTAP1 could acetylate histones H2A and H3 during early infection, thereby promoting susceptibility to P. sojae. In the absence of PsAvh52, GmTAP1 remained confined to the cytoplasm and did not modify plant susceptibility. These results demonstrate that GmTAP1 is a susceptibility factor that is hijacked by PsAvh52 in order to promote epigenetic modifications that enhance the susceptibility of soybean to P. sojae infection.

scholarly journals Nontoxic Nep1-Like Proteins of the Downy Mildew Pathogen Hyaloperonospora arabidopsidis: Repression of Necrosis-Inducing Activity by a Surface-Exposed Region

2012 ◽  
Vol 25 (5) ◽  
pp. 697-708 ◽  
Author(s):  
Adriana Cabral ◽  
Stan Oome ◽  
Nick Sander ◽  
Isabell Küfner ◽  
Thorsten Nürnberger ◽  
...  
Keyword(s):  
Amino Acids ◽  
Downy Mildew ◽  
Plant Pathogens ◽  
Exposed Region ◽  
Alternative Function ◽  
Early Expression ◽  
Specific Expansion ◽  
Species Specific ◽  
Hyaloperonospora Arabidopsidis ◽  
Specific Cluster

The genome of the downy mildew pathogen Hyaloperonospora arabidopsidis encodes necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP). Although NLP are widely distributed in eukaryotic and prokaryotic plant pathogens, it was surprising to find these proteins in the obligate biotrophic oomycete H. arabidopsidis. Therefore, we analyzed the H. arabidopsidis NLP (HaNLP) family and identified 12 HaNLP genes and 15 pseudogenes. Most of the 27 genes form an H. arabidopsidis–specific cluster when compared with other oomycete NLP genes, suggesting this class of effectors has recently expanded in H. arabidopsidis. HaNLP transcripts were mainly detected during early infection stages. Agrobacterium tumefaciens–mediated transient expression and infiltration of recombinant NLP into tobacco and Arabidopsis leaves revealed that all HaNLP tested are noncytotoxic proteins. Even HaNLP3, which is most similar to necrosis-inducing NLP proteins of other oomycetes and which contains all amino acids that are critical for necrosis-inducing activity, did not induce necrosis. Chimeras constructed between HaNLP3 and the necrosis-inducing PsojNIP protein demonstrated that most of the HaNLP3 protein is functionally equivalent to PsojNIP, except for an exposed domain that prevents necrosis induction. The early expression and species-specific expansion of the HaNLP genes is suggestive of an alternative function of noncytolytic NLP proteins during biotrophic infection of plants.

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