Viromics Unveils Extraordinary Genetic Diversity of the Family Closteroviridae in Wild Citrus

Abstract Background Our knowledge of citrus viruses is largely skewed toward virus pathology in cultivated orchards; comparatively little is known about the virus diversity and ecology in natural ecosystems. The metatranscriptomics approach were used to analyze wild citrus from the Ailao Mountain region in China, a region embracing huge biodiversity in an area where citrus species originated. We investigated the evolutionary history of citrus viruses to identify the factors facilitating outbreaks of emerging viruses. Results An independent wild citrus habitat were identified where citrus tristeza virus (CTV) exists along with three novel monopartite, graft-transmissible members of the family Closteroviridae differing from the managed agricultural systems that harbor other diverse citrus viruses. The viruses analyzed in 16 sequencing libraries of 32 citrus samples comprised five CTV genotypes, two inferred new ampelovirus species, and a monopartite ancestor type of the multipartite crinivirus that may represent a new taxon. Acquisition of heat shock protein genes (all viruses) and coat protein duplication (most), exchange of other exogenous genes (some), and alteration of expression strategy (rare) may reflect the significant historical nodes through which a Closteroviridae ancestor as the relic species has flourished. During viral expansion, genetic mutation coupled with recombination may be the essential impetus to update best-adapted sequences, as in the cases of our CTV and one of the ampeloviruses. Conclusions This research represents the first time of virus diversity in wild citrus. The findings deepen our knowledge of Closteroviridae modular evolution and diversification. Given the potential emergence of similar novel viruses as pathogens, the need for surveillance of their pathogenic and epidemiological characteristics and the presence of other novel citrus viruses among wild citrus is of utmost priority for global citrus production.