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Cited by 19Plant-Microbe Interactions and ImmunityFungal and yeast genetics researchImmune Response and Inflammation

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Exploring a diverse world of effector domains and amyloid signaling motifs in fungal NLR proteins

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Wojciechowski, Jakub W., Tekoglu, Emirhan, Gąsior-Głogowska, Marlena, Coustou, Virginie, Szulc, Natalia, Szefczyk, Monika, Kopaczyńska, Marta, Saupe, Sven J., Dyrka, Witold·2022·PLOS Computational Biology
DOI 10.1371/journal.pcbi.1010787PMC PMC9815663

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Abstract

NLR proteins are intracellular receptors constituting a conserved component of the innate immune system of cellular organisms. In fungi, NLRs are characterized by high diversity of architectures and presence of amyloid signaling. Here, we explore the diverse world of effector and signaling domains of fungal NLRs using state-of-the-art bioinformatic methods including MMseqs2 for fast clustering, probabilistic context-free grammars for sequence analysis, and AlphaFold2 deep neural networks for structure prediction. In addition to substantially improving the overall annotation, especially in basidiomycetes, the study identifies novel domains and reveals the structural similarity of MLKL-related HeLo- and Goodbye-like domains forming the most abundant superfamily of fungal NLR effectors. Moreover, compared to previous studies, we found several times more amyloid motif instances, including novel families, and validated aggregating and prion-forming properties of the most abundant of them in vitro and in vivo . Also, through an extensive in silico search, the NLR-associated amyloid signaling was identified in basidiomycetes. The emerging picture highlights similarities and differences in the NLR architectures and amyloid signaling in ascomycetes, basidiomycetes and other branches of life.

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Fig 1 Fungal NLR N-termini. a) Major general architectures; b) N-termini length distribution with taxonomic division, c) Same data scaled to 100% for each length range; Annotation coverage with regard to d) N-terminus length, e) taxonomic division; f) Annotation coverage of the MMSeqs clustered N-termini with regard to presence of taxonomically distant homologs in UniRef top hits (see Results). Euk. denotes Eukaryota, off Euk. category includes Bacteria, Archaea and Viruses. Colored bars indicate fraction of Pfam & inhouse annotated sequences (blue: only direct Pfam hits, violet: direct and with clustering & HHblits, rose: only with clustering & HHblits). Inhouse profiles were used only for direct Pfam searches. g) Distribution of domain families. Additional non-Pfam annotations included, see Results and Methods. N-termini shorter than 20 amino acids are distinguished, as unlikely to contain functional domains.
Fig 1 Fungal NLR N-termini. a) Major general architectures; b) N-termini length distribution with taxonomic division, c) Same data scaled to 100% for each length range; Annotation coverage with regard to d) N-terminus length, e) taxonomic division; f) Annotation coverage of the MMSeqs clustered N-termini with regard to presence of taxonomically distant homologs in UniRef top hits (see Results). Euk. denotes Eukaryota, off Euk. category includes Bacteria, Archaea and Viruses. Colored bars indicate fraction of Pfam & inhouse annotated sequences (blue: only direct Pfam hits, violet: direct and with clustering & HHblits, rose: only with clustering & HHblits). Inhouse profiles were used only for direct Pfam searches. g) Distribution of domain families. Additional non-Pfam annotations included, see Results and Methods. N-termini shorter than 20 amino acids are distinguished, as unlikely to contain functional domains.CC BY · PubMed Central
Fig 2 MLKL-like N-termini. a) Fingerprint alignment of the doubly (Goodbye-like & Helo-like) annotated OBZ65626 cluster including non-redundant sequences with direct Pfam annotations. The alignment was truncated C-terminally. Darker shade implies higher conservation, while gaps are represented as lines. Columns matched with Pfam profiles of MLKL-like domains are indicated with brown bars. Columns corresponding to helices in a predicted OBZ65626 model are indicated with solid magenta boxes. Columns alignable to the human MLKL structure are framed with a brown dashed line. Columns corresponding to helices in the aligned MLKL structure are indicated with dashed magenta boxes. b) The human MLKL structure (pdb:6zvoA). c) Structural models of various MLKL-like domains predicted with AlphaFold2 (see Methods). Regions aligned to the human MLKL structure with TM-align are shown in brown. Rainbow colors indicate model quality in terms of pLDDT (below or 50: red, 60: yellow, 70: green, 80: cyan, above 90: blue).
Fig 2 MLKL-like N-termini. a) Fingerprint alignment of the doubly (Goodbye-like & Helo-like) annotated OBZ65626 cluster including non-redundant sequences with direct Pfam annotations. The alignment was truncated C-terminally. Darker shade implies higher conservation, while gaps are represented as lines. Columns matched with Pfam profiles of MLKL-like domains are indicated with brown bars. Columns corresponding to helices in a predicted OBZ65626 model are indicated with solid magenta boxes. Columns alignable to the human MLKL structure are framed with a brown dashed line. Columns corresponding to helices in the aligned MLKL structure are indicated with dashed magenta boxes. b) The human MLKL structure (pdb:6zvoA). c) Structural models of various MLKL-like domains predicted with AlphaFold2 (see Methods). Regions aligned to the human MLKL structure with TM-align are shown in brown. Rainbow colors indicate model quality in terms of pLDDT (below or 50: red, 60: yellow, 70: green, 80: cyan, above 90: blue).CC BY · PubMed Central
Fig 3 Amyloid-like motifs in short N-termini of NLRs. Clusters of N-termini containing sequences resembling bacterial amyloid signaling motifs were identified using a probabilistic grammatical model [52]. Motifs were extracted with MEME [88] and iteratively refined with profile HMMs. (a) Profile HMM-based motif logos—grouped according to overlapping hits in NLR N-termini, as shown in panel (b) Overlapping hits in NLR N-termini. See Results and Methods for details. (c) Stacked histogram of motif hits positions in NLR N-termini for the five largest motif families, color-coded as in panel (a)).
Fig 3 Amyloid-like motifs in short N-termini of NLRs. Clusters of N-termini containing sequences resembling bacterial amyloid signaling motifs were identified using a probabilistic grammatical model [52]. Motifs were extracted with MEME [88] and iteratively refined with profile HMMs. (a) Profile HMM-based motif logos—grouped according to overlapping hits in NLR N-termini, as shown in panel (b) Overlapping hits in NLR N-termini. See Results and Methods for details. (c) Stacked histogram of motif hits positions in NLR N-termini for the five largest motif families, color-coded as in panel (a)).CC BY · PubMed Central
Fig 4 Potentially interacting amyloid-like motifs in Agaricomycetes. (a) Motif logos, sequence alignments and domain architectures of selected motif instances. (b) Schematic representation of a cluster of amyloid-like motifs in contig SPHSTscaffold_52 from genome assembly GCA_000827215.1 of Sphaerobolus stellatus SS14. (c) Multiple sequence alignment of motif instances in (b).
Fig 4 Potentially interacting amyloid-like motifs in Agaricomycetes. (a) Motif logos, sequence alignments and domain architectures of selected motif instances. (b) Schematic representation of a cluster of amyloid-like motifs in contig SPHSTscaffold_52 from genome assembly GCA_000827215.1 of Sphaerobolus stellatus SS14. (c) Multiple sequence alignment of motif instances in (b).CC BY · PubMed Central
Fig 5 The PUASM motif. Alignment of the PUASM sequence pairs (a) from effector C-terminus (left) and NLR N-terminus (right). Colors indicate residue hydrophobicity, curly brackets—the motif ranges. Deconvolution of ATR–FTIR spectra of air-dried peptide films of EQB50682.1_332_355 (bc) and EQB50683.1_9_31 (de) in the amide bands region (1750–1500 cm−1). Spectra registered at 20°C (68°F) after dissolving (bd) or after 40 days of incubation at 37°C (98.6°F) (ce). AFM images with cross-section profiles of peptides EQB50682.1_332_355 (fh) and EQB50683.1_9_31 (gi). Samples imaged after dissolving (fg) or after 40 days of incubation at 37°C (98.6°F) (hi).
Fig 5 The PUASM motif. Alignment of the PUASM sequence pairs (a) from effector C-terminus (left) and NLR N-terminus (right). Colors indicate residue hydrophobicity, curly brackets—the motif ranges. Deconvolution of ATR–FTIR spectra of air-dried peptide films of EQB50682.1_332_355 (bc) and EQB50683.1_9_31 (de) in the amide bands region (1750–1500 cm−1). Spectra registered at 20°C (68°F) after dissolving (bd) or after 40 days of incubation at 37°C (98.6°F) (ce). AFM images with cross-section profiles of peptides EQB50682.1_332_355 (fh) and EQB50683.1_9_31 (gi). Samples imaged after dissolving (fg) or after 40 days of incubation at 37°C (98.6°F) (hi).CC BY · PubMed Central
Fig 6 Expression of GFP/RFP-fused PUASM motifs in Podospora anserina. a) Micrographs of P. anserina strains expressing molecular fusions of PUASM with GFP or RFP, as indicated on the left; scale bar: 5 μm. Strains were analyzed in their initial state after transfection (left panels marked) and either after several days of subculturing (middle panels, spontanous foci formation) or after cytoplasmic contact with a strain expressing GFP–PUASM in the foci state (right panels, induced foci formation). Note that the GFP–PUASM construct (but not PUASM–RFP and PUASM–GFP) leads to spontaneous and induced foci-formation. Quantification of the rate of foci formation is given in Table F in S1 Text. b) Micrographs of strains expressing GFP–BASS3—positive control for the spontanous foci formation (BASS3 motif of WP_037701008.1 of Streptomyces atratus, positions 70 to 124, left panel), and two GFP–BASS3 mutants—negative controls (Q113P, middle, and Q120P, right panel).
Fig 6 Expression of GFP/RFP-fused PUASM motifs in Podospora anserina. a) Micrographs of P. anserina strains expressing molecular fusions of PUASM with GFP or RFP, as indicated on the left; scale bar: 5 μm. Strains were analyzed in their initial state after transfection (left panels marked) and either after several days of subculturing (middle panels, spontanous foci formation) or after cytoplasmic contact with a strain expressing GFP–PUASM in the foci state (right panels, induced foci formation). Note that the GFP–PUASM construct (but not PUASM–RFP and PUASM–GFP) leads to spontaneous and induced foci-formation. Quantification of the rate of foci formation is given in Table F in S1 Text. b) Micrographs of strains expressing GFP–BASS3—positive control for the spontanous foci formation (BASS3 motif of WP_037701008.1 of Streptomyces atratus, positions 70 to 124, left panel), and two GFP–BASS3 mutants—negative controls (Q113P, middle, and Q120P, right panel).CC BY · PubMed Central

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Metadata

Authors
Wojciechowski, J. W., Tekoglu, E., Gąsior-Głogowska, M., Coustou, V., Szulc, N., Szefczyk, M., Kopaczyńska, M., Saupe, S. J., & Dyrka, W.
Affiliations
  • Wrocław University of Science and Technology (PL)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
  • Saupe, Sven J.
  • Dyrka, Witold
ORCID
Venue
PLOS Computational Biology
Publisher
Public Library of Science (PLoS)
Published
2022-12-21
Volume
18
Issue
12
Pages
e1010787
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
DOI
10.1371/journal.pcbi.1010787
PMC
PMC9815663
OpenAlex
W4312064942
Cited by
19
References
5
Citations by year
2026: 2 · 2025: 10 · 2024: 1 · 2023: 6
FWCI
2.34
Type
journal article
Language
en
Update notices
new_version (2023-01-05)
Open access
Licence
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Digital Collections portal (Koç University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Narodowe Centrum Nauki (2019/35/B/NZ2/03997)
  • Wroclawskie Centrum Sieciowo-Superkomputerowe, Politechnika Wroclawska (98)
  • Narodowe Centrum Badań i Rozwoju (POWR.03.02.00-00-I003/16)
  • Agence Nationale de la Recherche (SFAS, R-17-CE11-0035)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords
NLR proteins, effector domain, Basidiomycota, Ascomycota, prion formation, protein aggregation, domain architecture, protein structure prediction, sequence clustering
MeSH terms
NLR Proteins, Amyloid, Fungal Proteins, Amyloidogenic Proteins

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