Parallel Evolution of C-Type Lectin Domain Gene Family Sizes in Insect-Vectored Nematodes

Abstract

The dispersal stage of pathogens is crucial for the successful spread and infection of their hosts. Some plant-parasitic nematodes (PPNs) have evolved specialized dispersal stages to reach healthy hosts by being carried out by insect vectors. Because gene gain and loss is a major factor contributing to the evolution of novel characteristics, it is essential to clarify the gene family characteristics among nematodes with different dispersal modes to disentangle the evolution of insect-mediated dispersal. Here, the size of the C-type lectin (CTL) family genes of insect-vectored nematodes was found to be drastically reduced compared with those of self-dispersing nematodes, whereas the diversity of their functional domains was significantly higher. The gene family sizes of vector-dispersed nematodes were only a twentieth of the size of that of a self-dispersing (i.e., without a biotic vector) nematode model Caenorhabditis elegans, and these genes were inactive during the dispersal stage. Phylogenetic analysis showed that some CTL genes of vector-borne PPNs shared higher homology to the animal parasitic nematodes compared with other PPNs. Moreover, homology modeling predicted that the CTLs of insect-vectored nematodes bear remarkable structural similarity to the lectin genes of their vector's immune system. Because CTL genes are important sugar-binding proteins for the innate immune response of C. elegans, the loss of some CTL genes of vector-transmitted PPNs might be responsible for their parallel adaptations to a mutualistic relationship with their vector. These results expand our understanding of the evolutionary benefits of vector-mediated transmission for the nematode and vector-nematode co-evolution.

A Genomic and Transcriptomic Analysis of the C-Type Lectin Gene Family Reveals Highly Expanded and Diversified Repertoires in Bivalves

“…The specificity of innate immunity has been demonstrated to be generated and maintained by the expanded CTL repertoires of several invertebrates, such as insects, crustaceans, and nematodes [53]. In particular, nematodes represent a good example of the relationship between the CTL gene family and the functional needs of the lifestyle of each species, as the size and domain diversity of CTL repertoires in insect-vectored nematodes was dramatically reduced compared to free-living species [57].…”