Evolutionary history of the NLR gene families across lophotrochozoans

Abstract

NOD-like receptor (NLR) genes are critical innate immune receptors in animals and plants. Lophotrochozoans represent one of the most species-rich superphyla that includes molluscs, segmented worms, flatworms, bryozoans, and other invertebrates, which is crucial to our understanding of immune system evolution in bilaterians. However, NLRs have not been systematically described in lophotrochozoans. We annotated 185 NLRs in 29 lophotrochozoan genomes, and analyzed their domain organization, phylogenetic distribution, molecular evolution, and gene expression. We found that all the 24 molluscan genomes studied encoded no more than three NLRs. None of these molluscan NLRs represented an inducible expression pattern under the infection of eight pathogens; some molluscan NLRs showed developmental stage-specific expression patterns. Instead, 29 molluscan incomplete NLR (incNLR) genes, encoding for proteins absent in the NACHT domain were upregulated under pathogen infection. We also documented the species-specific expansion of NLRs in the clades Polychaeta and Pteriidae. Our study revealed that gene duplication, domain shuffling, gene loss, and novel expression pattern played important roles in the molecular evolution of NLRs.