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Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens - PubMed

  • ️Fri Jan 01 2016

Comparative Study

Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens

Panagiotis F Sarris et al. BMC Biol. 2016.

Abstract

Background: Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Intracellular plant immune receptors called nucleotide-binding leucine-rich repeat (NLR) proteins contain a central nucleotide-binding (NB) domain followed by a series of leucine-rich repeats (LRRs), and are key initiators of plant defense responses. However, recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity. These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as "baits" for the pathogen-derived effector proteins, thus enabling pathogen recognition. Several names have been proposed to describe these proteins, including "integrated decoys" and "integrated sensors". We adopt and argue for "integrated domains" or NLR-IDs, which describes the product of the fusion without assigning a universal mode of action.

Results: We have scanned available plant genome sequences for the full spectrum of NLR-IDs to evaluate the diversity of integrations of potential sensor/decoy domains across flowering plants, including 19 crop species. We manually curated wheat and brassicas and experimentally validated a subset of NLR-IDs in wild and cultivated wheat varieties. We have examined NLR fusions that occur in multiple plant families and identified that some domains show re-occurring integration across lineages. Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen. While some of the integrated domains have been previously implicated in disease resistance, others provide new targets for engineering durable resistance to plant pathogens.

Conclusions: We have built a robust reproducible pipeline for detecting variable domain architectures in plant immune receptors across species. We hypothesize that NLR-IDs that we revealed provide clues to the host proteins targeted by pathogens, and that this information can be deployed to discover new sources of disease resistance.

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Figures

Fig. 1
Fig. 1

Phylogeny of the plant species and corresponding number of detected NLR and NLR-fusion proteins. The phylogeny of the plants used in the analyses was constructed using their corresponding NCBI taxon identification numbers. For the summary of NLR-IDs detected in each species, see Table 1 and Additional files 2 and 3. Annotation of all domains in NB-ARC-containing proteins and NLR-IDs and corresponding FASTA sequences are included in Additional files 4, 5, 6 and 7. NB: NB-ARC domain-containing proteins; NB-ID: NB-ARC plus any other canonical domains together with non-canonical domains; NLR: subset of NB with clearly identified LRRs; TLR: TIR-NB-ARC-LRR proteins; TN: TIR-NB-ARC proteins; T2N: TIR2-NB-ARC proteins

Fig. 2
Fig. 2

Word cloud analysis of the putative sensor domains found in fusion to NLRs. The word cloud represents relative abundance of different domains found in fusion. To correct for biases of sequencing particular plant families, word cloud was constructed on the plant family level (list of all domains occurring in NLR-ID in each plant family)

Fig. 3
Fig. 3

Overlap between IDs and domains present in host targets of plant pathogens. a An overlap between NLR-IDs from this study and functional domains present in the published Arabidopsis “effector interactome”. b Two examples of NLRs and their guardees, RIN4 and Exo70, that are known to be targeted by effectors in rice and Arabidopsis and which are found as fusions in other plant species

Fig. 4
Fig. 4

Domain architectures and structural analyses of NLR-kinase fusions. a Distribution of identified integrated kinase domains. b Complex fusions of domains on top of NLR-kinases. c Three-dimensional structural model of the kinase domain of an Arabidopsis NLR-kinase At4G12020 (aa 8–258) modelled after the best structural match, human serine/threonine protein kinase PAK 6 (PDB: 2C30). Conservation profile across all plant kinases found in NLR-IDs is overlapped on the structure, with most conserved residues depicted in red and most divergent in blue. d Zoom-in on the active site and its critical lysine and aspartate residues and a corresponding alignment logo show that the active site of kinases is completely conserved across all fusions

Fig. 5
Fig. 5

Evolutionary analyses of the WRKY domain in NLR-WRKYs family. a Multiple sequence alignment logo of the WRKY domains found in all NLR-IDs shows conserved core structural tryptophan and incomplete conservation of tyrosine and lysine that have been shown to be essential for recognizing the W-box DNA. b Maximum likelihood phylogeny of all Arabidopsis WRKY domain-containing proteins (black nodes) and the WRKYs detected as fusions in all flowering plants (strawberry nodes). Distinct Arabidopsis WRKY clades that form fusions are highlighted as the following: green, RRS1 clade; yellow, WRKY46; pink, WRKY70 and WRKY54; blue, WRKY16; and purple, WRKY19/MEKK4. Arabidopsis WRKY41 known to be the host target is marked with red asterisk

Fig. 6
Fig. 6

Summary of the information encoded in the discovered NLRs that possess “integrated domains”

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