Highlights d Species-wide NLR diversity is high but not unlimited d A large fraction of NLR diversity is recovered with 40-50 accessions d Presence/absence variation in NLRs is widespread, resulting in a mosaic population d A high diversity of NLR-integrated domains favor known virulence targets
Although the concept of botanical carnivory has been known since Darwin's time, the molecular mechanisms that allow animal feeding remain unknown, primarily due to a complete lack of genomic information. Here, we show that the transcriptomic landscape of the Dionaea trap is dramatically shifted toward signal transduction and nutrient transport upon insect feeding, with touch hormone signaling and protein secretion prevailing. At the same time, a massive induction of general defense responses is accompanied by the repression of cell death–related genes/processes. We hypothesize that the carnivory syndrome of Dionaea evolved by exaptation of ancient defense pathways, replacing cell death with nutrient acquisition.
In many plant species, conflicts between divergent elements of the immune system, especially nucleotide-binding oligomerization domain-like receptors (NLR), can lead to hybrid necrosis. Here, we report deleterious allele-specific interactions between an NLR and a non-NLR gene cluster, resulting in not one, but multiple hybrid necrosis cases in Arabidopsis thaliana . The NLR cluster is RESISTANCE TO PERONOSPORA PARASITICA 7 ( RPP7 ), which can confer strain-specific resistance to oomycetes. The non-NLR cluster is RESISTANCE TO POWDERY MILDEW 8 ( RPW8 ) / HOMOLOG OF RPW8 ( HR ), which can confer broad-spectrum resistance to both fungi and oomycetes. RPW8/HR proteins contain at the N-terminus a potential transmembrane domain, followed by a specific coiled-coil (CC) domain that is similar to a domain found in pore-forming toxins MLKL and HET-S from mammals and fungi. C-terminal to the CC domain is a variable number of 21- or 14-amino acid repeats, reminiscent of regulatory 21-amino acid repeats in fungal HET-S. The number of repeats in different RPW8/HR proteins along with the sequence of a short C-terminal tail predicts their ability to activate immunity in combination with specific RPP7 partners. Whether a larger or smaller number of repeats is more dangerous depends on the specific RPW8/HR autoimmune risk variant.
24Disease is both among the most important selection pressures in nature and among the 25 main causes of yield loss in agriculture. In plants, resistance to disease is often conferred by 26Nucleotide-binding Leucine-rich Repeat (NLR) proteins. These proteins function as 27 intracellular immune receptors that recognize pathogen proteins and their effects on the 28 plant. Consistent with evolutionarily dynamic interactions between plants and pathogens, 29NLRs are known to be encoded by one of the most variable gene families in plants, but the 30 true extent of intraspecific NLR diversity has been unclear. Here, we define the majority of 31the Arabidopsis thaliana species-wide "NLRome". From NLR sequence enrichment and 32 long-read sequencing of 65 diverse A. thaliana accessions, we infer that the pan-NLRome 33saturates with approximately 40 accessions. Despite the high diversity of NLRs, half of the 34 pan-NLRome is present in most accessions. We chart the architectural diversity of NLR 35 proteins, identify novel architectures, and quantify the selective forces that act on specific 36NLRs, domains, and positions. Our study provides a blueprint for defining the pan-NLRome 37 of plant species. 38 these mechanisms have been directly demonstrated only for a very small number of NLRs, 57 and additional mechanisms might await discovery. 58 59To date, NLR complements, or NLRomes, have been defined from available genome 60 annotations for single cultivars of plants or for multiple species across different taxonomic 61 levels, respectively 2,4,26-29 . The most striking findings were the repetitive modular 62 arrangement of NLRs and the discovery of head-to-head paired NLR genes, of which one 63 member included an ID 2,4,22,[26][27][28] . The potential use of those IDs as modular building blocks 64 has opened new possibilities for the engineering of novel resistances to pathogens [30][31][32][33] . The 65 existing list of IDs, however, likely represents only a glimpse of the true diversity across 66 plants. 67 68The definition of pan-NLRomes, or repertoires of NLR genes, across different species, or 69 higher taxonomic groups, has provided estimates of the variation in size of the NLR family 34-70 36 , presence/absence relations 35,36 , categorical distribution into structural classes across the 71
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