Solution NMR Structures of Pyrenophora tritici-repentis ToxB and Its Inactive Homolog Reveal Potential Determinants of Toxin Activity

Nyarko, Afua; Singarapu, Kiran Kumar; Figueroa, Melania; Manning, Viola A.; Pandelova, Iovanna; Wolpert, T.; Ciuffetti, Lynda M.; Barbar, Elisar

doi:10.1074/jbc.m114.569103

Cited by 39 publications

(33 citation statements)

References 38 publications

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“…An emerging insight from these structures is the 392 existence of conserved folds despite originating from fungi that belong to different taxa and having 393 high levels of sequence diversity (reviewed by (Franceschetti et al, 2017)). An example is the 394 MAX (Magnaporthe Avrs and ToxB-like) effector family, which includes representatives from 395 the rice blast pathogen M. oryzae (Zhang et al, 2013;de Guillen et al, 2015;Maqbool et al, 2015;396 Ose et al, 2015) and the wheat pathogen Pyrenophora tritici-repentis (Nyarko et al, 2014). Here, 397…”

Section: Discussion 386mentioning

confidence: 99%

The crystal structure of SnTox3 from the necrotrophic fungusParastagonospora nodorumreveals a unique effector fold and insights into Kex2 protease processing of fungal effectors

Outram

Sung

et al. 2020

Preprint

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SummaryPlant pathogens cause disease through secreted effector proteins, which act to modulate host physiology and promote infection. Typically, the sequences of effectors provide little functional information and further targeted experimentation is required. Here, we utilised a structure/function approach to study SnTox3, an effector from the necrotrophic fungal pathogen Parastagonospora nodorum, which causes cell death in wheat-lines carrying the sensitivity gene Snn3.We developed a workflow for the production of SnTox3 in a heterologous host that enabled crystal structure determination. We show this approach can be successfully applied to effectors from other pathogenic fungi. Complementing this, an in-silico study uncovered the prevalence of an expanded subclass of effectors from fungi.The β-barrel fold of SnTox3 is a novel fold among fungal effectors. We demonstrate that SnTox3 is a pre-pro-protein and that the protease Kex2 removes the pro-domain. Our in-silico studies suggest that Kex2-processed pro-domain (designated here as K2PP) effectors are common in fungi, and we demonstrate this experimentally for effectors from Fusarium oxysporum f sp. lycopersici.We propose that K2PP effectors are highly prevalent among fungal effectors. The identification and classification of K2PP effectors has broad implications for the approaches used to study their function in fungal virulence.

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Section: Discussion 386mentioning

confidence: 99%

The crystal structure of SnTox3 from the necrotrophic fungusParastagonospora nodorumreveals a unique effector fold and insights into Kex2 protease processing of fungal effectors

Outram

Sung

et al. 2020

Preprint

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“…Interestingly, the threedimensional structures of effector proteins revealed unexpected similarities between unrelated proteins. For example, three-dimensional structures of the M. oryzae effectors AVR-Pia, AVR1-CO39, AVR-PikD, and AvrPiz-t contain the same core fold, despite sharing no apparent sequence similarity ( Moreover, the host-selective toxin ToxB from Pyrenophora tritici-repentis, despite being derived from a phylogenetically distant pathogen, also contains the same fold-a six-stranded β-sandwich, comprised of two anti-parallel β-sheets (Nyarko et al 2014). de Guillen et al (2015) designated effectors containing this conserved β-sandwich core as "MAX effectors" (for M. oryzae AVRs and ToxB) and identified additional family members in various ascomycete fungi.…”

Section: Lesson 4 Appearances Can Be Deceiving: Sequence Unrelated Ementioning

confidence: 99%

Lessons in effector and NLR biology of plant-microbe systems

Białas

Zess

Concepcion

et al. 2017

Preprint

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A diversity of plant-associated organisms secrete effectors-proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeatcontaining (NLR) proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plantmicrobe systems.

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“…Although AVR-Pik, AVR-Pia, and AVR1-CO39 do not share sequence similarities, they share a highly similar three-dimensional structure characterized by a six b-sandwich fold also present in two other effectors: AvrPiz-t from M. oryzae and ToxB from the wheat pathogenic fungus Pyrenophora tritici repentis (Zhang et al, 2013;de Guillen et al, 2015;Maqbool et al, 2015;Nyarko et al, 2014). The corresponding, structurally related Magnaporthe Avr and ToxB effectors were termed MAX effectors.…”

Section: Introductionmentioning

confidence: 99%

Recognition of the Magnaporthe oryzae Effector AVR-Pia by the Decoy Domain of the Rice NLR Immune Receptor RGA5

et al. 2017

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Nucleotide binding domain and leucine-rich repeat proteins (NLRs) are important receptors in plant immunity that allow recognition of pathogen effectors. The rice (Oryza sativa) NLR RGA5 recognizes the Magnaporthe oryzae effector AVR-Pia through direct interaction. Here, we gained detailed insights into the molecular and structural bases of AVR-Pia-RGA5 interaction and the role of the RATX1 decoy domain of RGA5. NMR titration combined with in vitro and in vivo protein-protein interaction analyses identified the AVR-Pia interaction surface that binds to the RATX1 domain. Structure-informed AVR-Pia mutants showed that, although AVR-Pia associates with additional sites in RGA5, binding to the RATX1 domain is necessary for pathogen recognition but can be of moderate affinity. Therefore, RGA5-mediated resistance is highly resilient to mutations in the effector. We propose a model that explains such robust effector recognition as a consequence, and an advantage, of the combination of integrated decoy domains with additional independent effector-NLR interactions.

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Solution NMR Structures of Pyrenophora tritici-repentis ToxB and Its Inactive Homolog Reveal Potential Determinants of Toxin Activity

Cited by 39 publications

References 38 publications

The crystal structure of SnTox3 from the necrotrophic fungusParastagonospora nodorumreveals a unique effector fold and insights into Kex2 protease processing of fungal effectors

The crystal structure of SnTox3 from the necrotrophic fungusParastagonospora nodorumreveals a unique effector fold and insights into Kex2 protease processing of fungal effectors

Lessons in effector and NLR biology of plant-microbe systems

Recognition of the Magnaporthe oryzae Effector AVR-Pia by the Decoy Domain of the Rice NLR Immune Receptor RGA5

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