Prediction of effector protein structures from fungal phytopathogens enables evolutionary analyses

Nature Microbiology, Год журнала: 2023, Номер 8(1), С. 174 - 187

Опубликована: Янв. 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.

Язык: Английский

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Effector Identification in Plant Pathogens

Phytopathology, Год журнала: 2023, Номер 113(4), С. 637 - 650

Опубликована: Апрель 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.

Язык: Английский

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Computational Structural Genomics Unravels Common Folds and Novel Families in the Secretome of Fungal PhytopathogenMagnaporthe oryzae

Molecular Plant-Microbe Interactions, Год журнала: 2021, Номер 34(11), С. 1267 - 1280

Опубликована: Авг. 19, 2021

Structural biology has the potential to illuminate evolution of pathogen effectors and their commonalities that cannot be readily detected at primary sequence level. Recent breakthroughs in protein structure modeling have demonstrated feasibility predict folds without depending on homologous templates. These advances enabled a genome-wide computational structural approach help understand proteins based predicted folds. In this study, we employed prediction methods secretome destructive fungal

Язык: 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, Год журнала: 2023, Номер 120(32)

Опубликована: Июль 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

Язык: Английский

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Surface frustration re-patterning underlies the structural landscape and evolvability of fungal orphan candidate effectors

Nature Communications, Год журнала: 2023, Номер 14(1)

Опубликована: Авг. 28, 2023

Pathogens secrete effector proteins to subvert host physiology and cause disease. Effectors are engaged in a molecular arms race with the resulting conflicting evolutionary constraints manipulate cells without triggering immune responses. The mechanisms allowing effectors be at same time robust evolvable remain largely enigmatic. Here, we show that 62 conserved structure-related families encompass majority of fungal orphan candidates Pezizomycotina subphylum. These diversified through changes patterns thermodynamic frustration surface residues. underlying mutations tended increase robustness overall protein structure while switching potential binding interfaces. This mechanism could explain how maintained biological activity over long timespans different environments provides model for emergence sequence-unrelated structures.

Язык: Английский

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A pathogen effector FOLD diversified in symbiotic fungi

New Phytologist, Год журнала: 2023, Номер 239(3), С. 1127 - 1139

Опубликована: Май 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.

Язык: Английский

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A secreted protease-like protein in Zymoseptoria tritici is responsible for avirulence on Stb9 resistance gene in wheat

PLoS Pathogens, Год журнала: 2023, Номер 19(5), С. e1011376 - e1011376

Опубликована: Май 12, 2023

Zymoseptoria tritici is the fungal pathogen responsible for Septoria blotch on wheat. Disease outcome in this pathosystem partly determined by isolate-specific resistance, where wheat resistance genes recognize specific factors triggering an immune response. Despite large number of known genes, molecular determinants involved such cultivar-specific remain largely unknown. We identified avirulence factor AvrStb9 using association mapping and functional validation approaches. Pathotyping transgenic strains Stb9 cultivars, near isogenic lines populations, showed that interacts with gene, encodes unusually gene a predicted secretion signal protease domain. It belongs to S41 family conserved across different filamentous fungi Ascomycota class may constitute core effector. also among global Z. population carries multiple amino acid substitutions caused strong positive diversifying selection. These results demonstrate contribution 'atypical' effector protein role sequence diversification escape host recognition, adding our understanding host-pathogen interactions evolutionary processes underlying adaptation.

Язык: Английский

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

eLife, Год журнала: 2023, Номер 12

Опубликована: Июль 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.

Язык: Английский

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The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungi

BMC Biology, Год журнала: 2022, Номер 20(1)

Опубликована: Ноя. 3, 2022

Abstract Background Scab, caused by the biotrophic fungus Venturia inaequalis , is most economically important disease of apples worldwide. During infection, V. occupies subcuticular environment, where it secretes virulence factors, termed effectors, to promote host colonization. Consistent with other plant-pathogenic fungi, many these effectors are expected be non-enzymatic proteins, some which can recognized corresponding resistance proteins activate plant defences, thus acting as avirulence determinants. To develop durable control strategies against scab, a better understanding roles that effector play in promoting growth well activating, suppressing, or circumventing protein-mediated defences apple, required. Results We generated first comprehensive RNA-seq transcriptome during colonization apple. Analysis this revealed five temporal waves gene expression peaked early, mid, mid-late infection. While number genes encoding secreted, proteinaceous candidates (ECs) varied each wave, belonged Spectral clustering based on sequence similarity determined majority ECs expanded protein families. gain insights into function, tertiary structures were predicted using AlphaFold2. Strikingly, despite an absence similarity, have structural from including members MAX, LARS, ToxA and FOLD In addition, several ECs, EC family AvrLm6 Leptosphaeria maculans adopt KP6-like fold. Thus, fold represent another shared among fungi. Conclusions Our study reveals transcriptomic profile underpinning provides enriched list investigated for avirulence. Furthermore, our supports idea numerous sequence-unrelated across fungi share common folds. doing so, gives weight hypothesis fungal evolved ancestral through duplication, followed diversification, produce but structurally similar proteins.

Язык: Английский

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Molecular plant immunity against biotrophic, hemibiotrophic, and necrotrophic fungi

Essays in Biochemistry, Год журнала: 2022, Номер 66(5), С. 581 - 593

Опубликована: Май 19, 2022

Pathogenic fungi use diverse infection strategies to obtain nutrients from plants. Biotrophic feed only on living plant tissue, whereas necrotrophic kill host cells extract nutrients. To prevent disease, plants need distinguish between pathogens with different life cycles, as a successful defense against biotroph, which often involves programmed cell-death around the site of infection, is not an appropriate response some necrotrophs. Plants utilize vast collection extracellular and intracellular receptors detect signatures pathogen attack. In turn, are under strong selection mask or avoid certain receptor responses while enhancing manipulating other promote virulence. this review, we focus involved in resistance fungal highlight, examples, how strategy can determine if recognition effective at preventing disease.

Язык: Английский

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