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

Abstract

BackgroundPlants 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.ResultsWe 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0228-7) contains supplementary material, which is available to authorized users.

In silico analysis of the LRR receptor-like serine threonine kinases subfamily in Morus notabilis

“…A previous survey (Cesari et al, 2014) revealed similar and unique integrated domain fusions to LRR-containing proteins, commonly occurred in mosses and across numerous lineages of flowering plants, enabling by this way an efficient fungal recognition. According to Sarris et al, (2016) the most abundant group of domains fusions at LRR-containing proteins is involving the kinase domain found in receptor-like kinases that transducer PAMPtriggered immunity in plants; these findings are in line with our results, as such integrated domains were quite frequent in our M. notabilis LRR-RSTK dataset. The primary genomic assembly of M. notabilis (He et al, 2013) does not include any assembled chromosomes or linkage groups (Li et al, 2014), hence we could not test whether these genes are found at tandem clusters.…”

“…Furthermore, we observed evidence of various functional domains fusions, predominantly at the C-termini of M. notabilis LRR-RSTKs, mostly integrated by the Pkinase_Tyr and the Malectin or Malectin-like domains. Recent studies demonstrated that LRR-containing proteins with non-typical domain architectures, mainly these that are including "integrated decoys", play a crucial role in plant immunity with an integration re-occurring and an evolutionarily conserved pattern being evident across numerous species lineages (Sarris et al, 2016). A previous survey (Cesari et al, 2014) revealed similar and unique integrated domain fusions to LRR-containing proteins, commonly occurred in mosses and across numerous lineages of flowering plants, enabling by this way an efficient fungal recognition.…”

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

“…The most common domains match known integrated decoy domains 85,86 , but many more rare types were also found. The presence of specific domains in different NLR subfamilies point to multiple, independent acquisitions of decoys by NLRs (Supplementary Table 42).…”

Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins

“…Given that the HvWRKY1/2 and MYB6 transcription factors interact with the MLA10 CC domain (20,45), it is possible that these nuclear proteins are guardees/decoys that are necessary for effector perception. Indeed, recent findings suggest that transcription factors such as WRKY and MYB are common integrated domains/decoys in plant NLR proteins, indicating that they could be common effector targets (46)(47)(48). Previous yeast two-hybrid assays did not detect any interaction of the Sr33 CC domain with HvWRKY1, HvWRKY2, or their wheat orthologs (10).…”