Sympatric populations of crop and wild carrots (Daucus carota ssp.) have distinct viromes, with shared core species more prevalent in farm-grown populations

Abstract

Viral exchanges between crops and wild plants are important considerations in virus ecology and epidemiology but remain poorly understood. To investigate such exchanges, we compared the viromes of wild and farmed carrots (Daucus carota ssp.) growing near each other in France. Farm populations included cultivated varieties and off-type carrots (resembling wild ones) growing among them. This crop - wild relative pathosystem offers notable opportunities for virus exchange due to the hosts’ genetic closeness and geographic proximity. High-throughput sequencing found that viral taxonomic richness was greatest in wild carrots. However, hierarchical clustering and bipartite network analyses revealed that wild and farm carrot viromes differed in their seed-borne and vector-borne components. While ~50% of viral taxa were shared among carrot population types, others were uniquely associated with either wild or farm carrots. Individual-plant RT-PCR testing of 16 aphid-borne agents from the shared core virome found their prevalence was generally greatest in farm populations, with some geographic variability in virus pressure. The viromes of off-type and cultivated carrots were most similar, suggesting that proximity and/or management practices influence virome properties. For some aphid-borne viruses, similar isolates were found in wild and cultivated carrots, suggesting exchanges between them or with a shared source. However, isolates of other aphid-borne viruses clustered by carrot type, indicating barriers to viral fluxes, that might involve differential susceptibility of populations, vector preferences, or unidentified factors. To improve virus management, we need better understanding of how specific facilitators and barriers of viral exchange can be manipulated to reduce negative viral impacts.