Viromics unveils extraordinary genetic diversity of the family Closteroviridae in wild citrus

Abstract

Our knowledge of citrus viruses is largely skewed toward virus pathology in cultivated orchards. Little is known about the virus diversity in wild citrus species. Here, we used a metatranscriptomics approach to characterize the virus diversity in a wild citrus habitat within the proposed center of the origin of citrus plants. We discovered a total of 44 virus isolates that could be classified into species Citrus tristeza virus and putative species citrus associated ampelovirus 1, citrus associated ampelovirus 2, and citrus virus B within the family Closteroviridae, providing important information to explore the factors facilitating outbreaks of citrus viruses and the evolutionary history of the family Closteroviridae. We found that frequent horizontal gene transfer, gene duplication, and alteration of expression strategy have shaped the genome complexity and diversification of the family Closteroviridae. Recombination frequently occurred among distinct Closteroviridae members, thereby facilitating the evolution of Closteroviridae. Given the potential emergence of similar wild-citrus-originated novel viruses as pathogens, the need for surveillance of their pathogenic and epidemiological characteristics is of utmost priority for global citrus production.

Exotic and Emergent Citrus Viruses Relevant to the Mediterranean Region

“…They must be efficiently organized in order to allow proper control measures, based on the potential invader pathogenicity and epidemiological characteristics. This should become an utmost priority in the case of exotic pathogens vectored by insects or mechanically transmitted to different hosts-conditions that could generate significant genetic changes and potential new pathogens [155].…”

“…The advent of HTS technologies [159,160] has shown the potential advantage of providing a complete view of the phytosanitary status of plants and let to discriminate between new genetic variants [155,161]. It allows researchers to reduce costs and time, especially if compared to bioassays, which can require 2-3 years to develop symptoms.…”

A novel RNA virus, Thesium chinense closterovirus 1, identified by high-throughput RNA-sequencing of the parasitic plant Thesium chinense

“…Closteroviridae is a family of RNA viruses that infect plants, leading to considerable yield losses in commer cially important plants (beet, carrot, citrus, grape, rasp berry, strawberry, tobacco, and tomato) (Agranovsky et al, 1994;Karasev et al, 1995;Menzel et al, 2009;Martelli et al, 2012;Wang et al, 2016;Fiallo-Olive and Navas-Castillo, 2019;Martelli, 2019;Liu et al, 2021). The family Closteroviridae comprises of four known genera (Ampelovirus, Closterovirus, Crinivirus, and Velarivirus) and a group of unassigned species (Agranovsky, 2016;Martelli, 2019;Fuchs et al, 2020).…”

“…Transcriptome data from plant tissues often contain sequences originating from RNA viruses that symptomatically or asymptomatically infect the host plant (He et al, 2015;Susi et al, 2019;Liu et al, 2021;Quintanilha-Peixoto et al, 2021). Novel viral genome sequences can be identified by sequence comparisons of assembled plant transcriptome contigs and known viral protein sequences (Orilio et al, 2018;Bejerman et al, 2020;2021;Choi et al, 2021;Shin et al, 2021).…”

Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing

“…Recent technological advances have dramatically accelerated the pace of RNA virus discovery both on land and in the ocean [25][26][27][28]. One metagenomics approach that has been most successful in plants is virus discovery by deep sequencing and assembly of virus-derived siRNAs (vdSAR), which is based on the findings that the viral siRNAs produced by plant and invertebrate hosts overlap in sequence and can be assembled into the viral genome segments for virus discovery [29][30][31][32].…”