Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions

Abstract

Understanding evolution of plant immunity is necessary to inform rational approaches (Hall et al., 2009;Joshi et al., 2013).With over 50 fully sequenced plant genomes today, it is . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/100834 doi: bioRxiv preprint first posted online Jan. 20, 2017; Hotspots in Plant Immunity Gene Fusions 2 timely to apply comparative genomics approaches to investigate common trends in NLR evolution across the plant kingdom, including key crop species.In contrast to the highly conserved NB-ARC domains, the Leucine Rich Repeats (LRRs) of NLRs show high variability (Noel et al., 1999;Jacob, Vernaldi and Maekawa, 2013). The functional consequence of high LRR variation is thought to be the generation of novel recognition specificities (Bakker et al., 2006;Sukarta, Slootweg and Goverse, 2016). In addition, recent findings show that novel pathogen recognition specificities can also be acquired through the fusion of non-canonical domains to NLRs (Le Roux et al., 2015;Kroj et al., 2016). These exogenous domains can serve as 'baits' mimicking host targets of pathogen-derived effector molecules and therefore act in concert with LRR variation to broaden the spectra of recognised pathogenderived effectors (Cesari, Bernet al., 2014a; Cesari et al., 2014b;Le Roux et al., 2015).NLRs plant immune receptors were discovered over 20 years ago through cloning of plant disease resistance genes in Arabidopsis (Mindrinos et al., 1994; Bent et al., 1994) It is also clear that NLR(-ID) protein duplication has proliferated most strongly in these species for this hotspot clade ( Figure 1E). However, the relative ratio of NLRs with and without extra domains in this clade has remained relatively constant at around 59% suggesting that the rate of domain recycling has been constant across these species ( Figure 1B Expansion of the NLR-ID hotspot 1 clade is linked to diversification through new gene fusionsThe NLR-ID proteins from evolutionary hotspot 1 were examined further to test the hypothesis that the increase in the number of NLRs with integrated domains was due to the creation of novel gene fusions rather than the duplication of existing ID fusions. A clear expansion of the ID domain repertoire was found for this group of proteins, particularly for the Triticeae species (Table 1). It is possible that differences in the observed repertoires can be explained partly by incomplete annotation of genomes or fragmented assembly of NLRs; such proteins were omitted from the phylogenetic analysis if they were < 70 % complete across the NB-ARC domain.However, the overall trend across the genomes strongly suggests that differences cannot be explained solely by differences in genome assemblies. Moreover, genomes such as B. distachyon, Z. mays and O. sativa are assembled to much higher quality than those of the Triticeae species, yet they contain fewer NLR-IDs and have lower ID di...

RefPlantNLR: a comprehensive collection of experimentally validated plant NLRs

“…Of these non-canonical domains, the N-terminal late-blight resistance protein R1 domain (also known as the Solanaceae domain; Pfam signature PF12061) only occurs in association with the NB-ARC domain, and has an ancient origin likely in the most recent common ancestor of the Asterids and Amaranthaceae (Seong et al ., 2020). Other non-canonical domains are also more wide-spread, including the monocot-specific integration of a zinc-finger BED domain in between the CC and NB-ARC domain (Bailey et al ., 2018; Marchal et al ., 2018). Finally, some CC-NLRs have significantly truncated NB-ARC domain as is the case for Pb1 and RXL, the latter which using InterProScan only gets annotated with a LRR domain although it retains other NLR motifs such as the EDVID and RNBS-D motifs ( Figure 3C ).…”

The Plant “Resistosome”: Structural Insights into Immune Signaling

“…NLRs with Integrated Domains Many plant NLRs have been shown to include non-canonical integrated domains that act as baits for pathogen effectors. These domains are thought to be related to ancestral effector virulenceassociated targets (Bailey et al, 2018). Where characterized, these integrated domains bind directly to pathogen effectors.…”

The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity

“…Some of these host targets have been co-opted by plant intracellular nucleotide-binding leucine rich repeat (NLR) immune receptors to act as baits to detect pathogens, and are then known as integrated domains (IDs) (Cesari et al 2014; Wu et al 2015; Sarris et al 2016; Kroj et al 2016). Genome-wide bioinformatics searches have found these domains in diverse immune receptors from multiple plant families (Sarris et al 2016; Kroj et al 2016; Baggs et al 2017; Bailey et al, 2018). We hypothesize that such widespread NLR-IDs modulate basic immune responses that are conserved among plants.…”