A critical appraisal of DNA transfer from plants to parasitic cyst nematodes.

Abstract

Plant-parasitic nematodes are one of the most economically important pests of crops. It is widely accepted that Horizontal Gene Transfer (HGT) - the natural acquisition of foreign genes in parasitic nematodes - contributes to parasitism. However, an apparent paradox has emerged from HGT analyses: On one hand, distantly related organisms with very dissimilar genetic structures (i.e. bacteria), and only transient interactions with nematodes as far as we know, dominate the list of putative donors; while on the other hand, considerably more closely related organism (i.e. the host plant), with similar genetic structure (i.e. introns) and documented long-term associations with nematodes, are rare among the list of putative donors. Given that these nematodes ingest cytoplasm from a living plant cell for several weeks, there seems to be a conspicuous absence of plant-derived cases. Here we used comparative genomic approaches to evaluate possible plant-derived HGT events in plant parasitic nematodes. Our evidence supports a cautionary message for plant-derived HGT cases in the sugar beet cyst nematode, Heterodera schachtii. We propose a four step model for HGT from plant to parasite in order to evaluate why the absence of plant-derived HGT cases is observed. We find that the plant genome is mobilised by the nematode during infection, but that uptake of said "mobilome" is the first major barrier to HGT from host to nematode. These results provide new insight into our understanding of the prevalence/role of nucleic acids exchange in the arms race between plants and plant parasites.