The stem rust effector protein AvrSr50 escapes Sr50 recognition by a substitution in a single surface‐exposed residue

Ortiz, Diana; Chen, Jian; Outram, Megan A.; Saur, Isabel M. L.; Upadhyaya, Narayana M.; Mago, Rohit; Ericsson, Daniel; Césari, Stella; Chen, Chunhong; Williams, Simon J.; Dodds, Peter N.

doi:10.1111/nph.18011

Cited by 47 publications

(56 citation statements)

References 93 publications

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“…S10) (Sarma et al, 2005; Wang et al, 2007; Di et al, 2017). However, the structural comparison between experimentally determined AvrSr50 (Ortiz et al, 2022) and members in Cluster 171 supported greater structural similarity between the sequence-unrelated secreted proteins (Fig. 2E).…”

Section: Resultsmentioning

confidence: 85%

Comparative computational structural genomics highlights divergent evolution of fungal effectors

Seong

Krasileva

2022

Preprint

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Elucidating the evolution of pathogen effector molecules is critical to understand infection mechanisms of fungal phytopathogens and ensure crop security. However, rapid diversification that diminishes sequence similarities between homologous effectors has largely concealed the roots of effector evolution. We predicted the folds of 26,653 secreted proteins from 21 species with AlphaFold and performed structure-guided comparative analyses on two aspects of effector evolution: uniquely expanded effector families and common folds present across the fungal species. Extreme expansion of nearly lineage-specific effector families was found only in several obligate biotrophs, Blumeria graminis and Puccinia graminis. The highly expanded effector families were the source of conserved sequence motifs, such as the Y/F/WxC motif. We identified additional lineage-specific effector families that include known (a)virulence factors, such as AvrSr35, AvrSr50 and Tin2. These families represented new classes of sequence-unrelated structurally similar effectors. Structural comparisons revealed that the expanded structural folds further diversify through domain duplications and fusion with disordered stretches. Sub-and neo-functionalized structurally similar effectors reconverge on regulation, expanding the functional pools of effectors in the pathogen infection cycle. We also found evidence that many effector families could have originated from ancestral folds that have been conserved across fungi. Collectively, our study highlights diverse mechanisms of effector evolution and supports divergent evolution of effectors that leads to emergence of pathogen virulence from ancestral proteins.

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Section: Resultsmentioning

confidence: 85%

Comparative computational structural genomics highlights divergent evolution of fungal effectors

Seong

Krasileva

2022

Preprint

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“…Direct recognition of pathogen effectors by plant NLRs can be rapidly circumvented by polymorphisms of effector residues at the effector–NLR interface, particularly as a pathogen and its host plant typically evolve at different time scales. Virulent isolates of Pgt within and beyond the Ug99 lineage have escaped the recognition of at least one of the recently cloned Sr genes, including single amino acid changes in the effector 47 . For example, a Pgt isolate with combined virulence against Sr35 and Sr50 caused an epidemic in Sicily in 2017 48 .…”

Section: Discussionmentioning

confidence: 99%

A wheat resistosome defines common principles of immune receptor channels

Förderer

Lawson

et al. 2022

Nature

171

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Plant intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) detect pathogen effectors to trigger immune responses1. Indirect recognition of a pathogen effector by the dicotyledonous Arabidopsis thaliana coiled-coil domain containing NLR (CNL) ZAR1 induces the formation of a large hetero-oligomeric protein complex, termed the ZAR1 resistosome, which functions as a calcium channel required for ZAR1-mediated immunity2–4. Whether the resistosome and channel activities are conserved among plant CNLs remains unknown. Here we report the cryo-electron microscopy structure of the wheat CNL Sr355 in complex with the effector AvrSr356 of the wheat stem rust pathogen. Direct effector binding to the leucine-rich repeats of Sr35 results in the formation of a pentameric Sr35–AvrSr35 complex, which we term the Sr35 resistosome. Wheat Sr35 and Arabidopsis ZAR1 resistosomes bear striking structural similarities, including an arginine cluster in the leucine-rich repeats domain not previously recognized as conserved, which co-occurs and forms intramolecular interactions with the 'EDVID' motif in the coiled-coil domain. Electrophysiological measurements show that the Sr35 resistosome exhibits non-selective cation channel activity. These structural insights allowed us to generate new variants of closely related wheat and barley orphan NLRs that recognize AvrSr35. Our data support the evolutionary conservation of CNL resistosomes in plants and demonstrate proof of principle for structure-based engineering of NLRs for crop improvement.

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“…Direct recognition of pathogen effectors by plant NLRs can be rapidly circumvented by polymorphisms of effector residues at the effector–NLR interface, particularly as a pathogen and its host plant evolve at different time scales. Virulent isolates of Pgt within and beyond the Ug99 lineage have escaped the recognition of at least one of the recently cloned Sr genes, including single amino acid changes in the effector ( 44 ). For example, a Pgt isolate with combined virulence against Sr35 and Sr50 caused an epidemic in Sicily in 2017 ( 45 ).…”

Section: Discussionmentioning

confidence: 99%

A wheat resistosome defines common principles of immune receptor channels

Förderer

Lawson

et al. 2022

Preprint

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Plant intracellular nucleotide-binding leucine-rich repeat (NLRs) receptors detect pathogen effectors to trigger immune responses. Indirect recognition of a pathogen effector by the dicotyledonous Arabidopsis thaliana coiled-coil (CC) domain containing NLR (CNL) ZAR1 induces the formation of a large hetero-oligomeric protein complex, termed the ZAR1 resistosome, which functions as a calcium channel required for ZAR1-mediated immunity (1–3). Whether the resistosome and channel activities are conserved among plant CNLs remains unknown. We report here a cryogenic electron microscopy (cryo-EM) structure of the wheat CNL Sr35 in complex with the effector AvrSr35 of the wheat stem rust pathogen at 3.0 Å resolution. Direct effector binding to the leucine-rich repeats (LRRs) of Sr35 results in the formation of a pentameric Sr35-AvrSr35 complex, which we designate the Sr35 resistosome. Wheat Sr35 and Arabidopsis ZAR1 resistosomes bear striking structural similarity, including a previously unnoticed arginine cluster in the LRR domain that co-occurs and forms intramolecular interactions with the ‘EDVID’ motif in the CC domain. Electrophysiological measurements show that the Sr35 resistosome exhibits non-selective cation channel activity. These structural insights allowed us to generate novel variants of closely related wheat and barley orphan NLRs that recognize AvrSr35. Our data support the evolutionary conservation of CNL resistosomes in plants and demonstrate proof of principle for structure-based engineering of NLRs for crop improvement.

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The stem rust effector protein AvrSr50 escapes Sr50 recognition by a substitution in a single surface‐exposed residue

Cited by 47 publications

References 93 publications

Comparative computational structural genomics highlights divergent evolution of fungal effectors

Comparative computational structural genomics highlights divergent evolution of fungal effectors

A wheat resistosome defines common principles of immune receptor channels

A wheat resistosome defines common principles of immune receptor channels

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