Prediction of effector protein structures from fungal phytopathogens enables evolutionary analyses

Nature Microbiology, Journal Year: 2023, Volume and Issue: 8(1), P. 174 - 187

Published: Jan. 5, 2023

Elucidating the similarity and diversity of pathogen effectors is critical to understand their evolution across fungal phytopathogens. However, rapid divergence that diminishes sequence similarities between putatively homologous has largely concealed roots effector evolution. Here we modelled structures 26,653 secreted proteins from 14 agriculturally important phytopathogens, six non-pathogenic fungi one oomycete with AlphaFold 2. With 18,000 successfully predicted folds, performed structure-guided comparative analyses on two aspects evolution: uniquely expanded sequence-unrelated structurally similar (SUSS) families common folds present species. Extreme expansion lineage-specific SUSS was found only in several obligate biotrophs, Blumeria graminis Puccinia graminis. The highly were source conserved motifs, such as Y/F/WxC motif. We identified new classes include known virulence factors, AvrSr35, AvrSr50 Tin2. Structural comparisons revealed structural further diversify through domain duplications fusion disordered stretches. Putatively sub- neo-functionalized could reconverge regulation, expanding functional pools infection cycle. also evidence many have originated ancestral fungi. Collectively, our study highlights diverse mechanisms supports divergent a major force driving proteins.

Language: Английский

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Effector Identification in Plant Pathogens

Phytopathology, Journal Year: 2023, Volume and Issue: 113(4), P. 637 - 650

Published: April 1, 2023

Effectors play a central role in determining the outcome of plant-pathogen interactions. As key virulence proteins, effectors are collectively indispensable for disease development. By understanding mechanisms effectors, fundamental knowledge microbial pathogenesis and resistance have been revealed. also considered double-edged swords because some them activate immunity resistant plants after being recognized by specific immune receptors, which evolved to monitor pathogen presence or activity. Characterization effector recognition their cognate receptors downstream signaling pathways is instrumental implementing resistance. Over past decades, substantial research effort has focused on biology, especially concerning interactions with targets plant cells. A foundation this robust identification repertoire from given pathogen, depends heavily bioinformatic prediction. In review, we summarize methodologies that used mining various pathogens use different delivery mechanisms. We discuss current limitations provide perspectives how recently developed analytic tools technologies may facilitate hence generation more complete vision host-pathogen [Formula: see text] Copyright © 2023 The Author(s). This an open access article distributed under CC BY-NC-ND 4.0 International license.

Language: Английский

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Pathogen perception and signaling in plant immunity

The Plant Cell, Journal Year: 2024, Volume and Issue: 36(5), P. 1465 - 1481

Published: Jan. 23, 2024

Abstract Plant diseases are a constant and serious threat to agriculture ecological biodiversity. Plants possess sophisticated innate immunity system capable of detecting responding pathogen infection prevent disease. Our understanding this has grown enormously over the past century. Early genetic descriptions plant disease resistance virulence were embodied in gene-for-gene hypothesis, while physiological studies identified pathogen-derived elicitors that could trigger defense responses cells tissues. Molecular these phenomena have now coalesced into an integrated model involving cell surface intracellular detection specific molecules proteins culminating induction various cellular responses. Extracellular receptors engage distinct signaling processes but converge on many similar outputs with substantial evidence for integration pathways interdependent networks controlling outcomes. Many molecular details recognition known, providing opportunities bioengineering enhance protection from Here we provide overview current main principles immunity, emphasis key scientific milestones leading insights.

Language: Английский

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A potato late blight resistance gene protects against multiple Phytophthora species by recognizing a broadly conserved RXLR-WY effector

Molecular Plant, Journal Year: 2022, Volume and Issue: 15(9), P. 1457 - 1469

Published: July 31, 2022

Species of the genus Phytophthora, plant killer, cause disease and reduce yields in many crop plants. Although Resistance to Phytophthora infestans (Rpi) genes effective against potato late blight have been cloned, few cloned other species. Most Rpi encode nucleotide-binding domain, leucine-rich repeat-containing (NLR) immune receptor proteins that recognize RXLR (Arg-X-Leu-Arg) effectors. However, whether NLR can effectors from multiple species has rarely investigated. Here, we identified a new RXLR-WY effector AVRamr3 P. is recognized by Rpi-amr3 wild Solanaceae Solanum americanum. associates with planta. broadly conserved different species, recognition homologs activates resistance pathogens, including tobacco black shank cacao pod pathogens parasitica palmivora. thus first characterized gene acts or These findings suggest novel path redeploy known R important pathogens.

Language: Английский

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Structural polymorphisms within a common powdery mildew effector scaffold as a driver of coevolution with cereal immune receptors

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(32)

Published: July 31, 2023

In plants, host-pathogen coevolution often manifests in reciprocal, adaptive genetic changes through variations host nucleotide-binding leucine-rich repeat immune receptors (NLRs) and virulence-promoting pathogen effectors. grass powdery mildew (PM) fungi, an extreme expansion of a RNase-like effector family, termed RALPH, dominates the repertoire, with some members recognized as avirulence (AVR) effectors by cereal NLR receptors. We report structures sequence-unrelated barley PM AVR

Language: Английский

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A pathogen effector FOLD diversified in symbiotic fungi

New Phytologist, Journal Year: 2023, Volume and Issue: 239(3), P. 1127 - 1139

Published: May 31, 2023

Pathogenic fungi use secreted effector proteins to suppress immunity and support their infection, but effectors have also been reported from that engage in nutritional symbioses with plants. Sequence-based comparisons between pathogens symbiotic arbuscular mycorrhizal (AM) are hampered by the huge diversity of sequences even within closely related microbes. To find sequence-divergent structurally similar shared pathogenic fungi, we compared protein structure models AM fungus Rhizophagus irregularis known pathogen effectors. We identified structural similarity Fusarium oxysporum f. sp. lycopersici dual domain (FOLD) effectors, which occur low numbers several fungal pathogens. Contrastingly, FOLD genes (MycFOLDs) found enlarged diversified gene families higher levels positive selection C-terminal domains. Our model comparison suggests MycFOLDs carbohydrate-binding motifs. Different MycFOLD expressed during colonisation different hosts MycFOLD-17 transcripts accumulate plant intracellular arbuscules. The exclusive presence across unrelated plant-colonising inducible expression, lineage-specific sequence diversification arbuscules suggest act as fungi.

Language: Английский

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Pathogen protein modularity enables elaborate mimicry of a host phosphatase

Cell, Journal Year: 2023, Volume and Issue: 186(15), P. 3196 - 3207.e17

Published: June 26, 2023

Pathogens produce diverse effector proteins to manipulate host cellular processes. However, how functional diversity is generated in an repertoire poorly understood. Many effectors the devastating plant pathogen Phytophthora contain tandem repeats of "(L)WY" motif, which are structurally conserved but variable sequences. Here, we discovered a module formed by specific (L)WY-LWY combination multiple effectors, efficiently recruits serine/threonine protein phosphatase 2A (PP2A) core enzyme hosts. Crystal structure effector-PP2A complex shows that enables hijacking PP2A form holoenzymes. While sharing PP2A-interacting at amino terminus, these possess divergent C-terminal LWY units and regulate distinct sets phosphoproteins host. Our results highlight appropriation essential through molecular mimicry pathogens diversification promoted modularity repertoire.

Language: Английский

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The structural repertoire of Fusarium oxysporum f. sp. lycopersici effectors revealed by experimental and computational studies

eLife, Journal Year: 2023, Volume and Issue: 12

Published: July 18, 2023

Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface cytosolic receptors results activation of defence pathways and immunity. Despite their importance, our general understanding fungal effector immunity remains poor. One complication often associated with effectors is high sequence diversity lack identifiable motifs precluding prediction structure function. In recent years, several studies have demonstrated can be grouped into structural classes, despite significant variation existence across taxonomic groups. Using protein X-ray crystallography, we identify a new class hidden within secreted xylem (SIX) from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised Avr1 (SIX4) Avr3 (SIX1) represent founding members Fol dual-domain (FOLD) class, containing two distinct domains. AlphaFold2, predicted full SIX repertoire show SIX6 SIX13 are also FOLD which validated experimentally for SIX6. Based on comparisons, present three divisions fungi expanded symbionts. Further comparisons demonstrate secretes adopt limited number folds during infection tomato. This analysis revealed relationship between transcriptionally co-regulated pairs. We make use understand its I receptor, leads disease resistance study represents an important advance Fol-tomato, extension plant-fungal interactions, will assist development novel control engineering strategies combat pathogens.

Language: Английский

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Pathways to engineering plant intracellular NLR immune receptors

Current Opinion in Plant Biology, Journal Year: 2023, Volume and Issue: 74, P. 102380 - 102380

Published: May 15, 2023

Factors including climate change and increased global exchange are set to escalate the prevalence of plant diseases, posing an unprecedented threat food security making it more challenging meet demands ever-growing population. As such, new methods pathogen control essential help with growing danger crop losses diseases. The intracellular immune system plants utilizes nucleotide-binding leucine-rich repeat (NLR) receptors recognize activate defense responses virulence proteins (effectors) delivered host. Engineering recognition properties NLRs toward effectors is a genetic solution diseases high specificity, sustainable than several current for that frequently rely on agrochemicals. Here, we highlight pioneering approaches enhancing effector in discuss barriers solutions engineering system.

Language: Английский

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The synthetic NLR RGA5HMA5 requires multiple interfaces within and outside the integrated domain for effector recognition

Nature Communications, Journal Year: 2024, Volume and Issue: 15(1)

Published: Feb. 6, 2024

Abstract Some plant sensor nucleotide-binding leucine-rich repeat (NLR) receptors detect pathogen effectors through their integrated domains (IDs). Rice RGA5 NLR recognizes its corresponding AVR-Pia and AVR1-CO39 from the blast fungus Magnaporthe oryzae direct binding to heavy metal-associated (HMA) ID trigger RGA4 helper NLR-dependent resistance in rice. Here, we report a mutant of named HMA5 that confers complete transgenic rice plants M. strains expressing noncorresponding effector AVR-PikD. carries three engineered interfaces, two which lie HMA other C-terminal Lys-rich stretch tailing ID. However, variants having one or including replacing all Lys residues with Glu stretch, failed activate RGA4-dependent cell death protoplasts. Altogether, this work demonstrates NLRs require concerted action multiple surfaces within outside IDs both recognize NLR-mediated resistance, has implications structure-guided designing NLRs.

Language: Английский

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