Abstract
Despite the importance of viral strains/variants as agents of emerging diseases, genetic and evolutionary processes affecting their ecology are not fully understood. To get insight into this topic, we assessed the population and spatial dynamic parameters of citrus leprosis virus C (CiLV-C, genus Cilevirus, family Kitaviridae). CiLV-C is the etiological agent of citrus leprosis disease, a non-systemic infection considered the main viral disorder affecting citrus orchards in Brazil. Overall, we obtained 18 complete or near-complete viral genomes, 123 complete nucleotide sequences of the open reading frame (ORF) encoding the putative coat protein, and 204 partial nucleotide sequences of the ORF encoding the movement protein, from 430 infected Citrus spp. samples collected between 1932 and 2020. A thorough examination of the collected dataset suggested that the CiLV-C population consists of the major lineages CRD and SJP, unevenly distributed, plus a third one called ASU identified in this work, which is represented by a single isolate found in an herbarium sample collected in Asuncion, Paraguay, in 1937. Viruses from the three lineages share about 85% nucleotide sequence identity and show signs of inter-clade recombination events. Members of the lineage CRD were identified both in commercial and non-commercial citrus orchards. However, those of the lineages SJP were exclusively detected in samples collected in the citrus belt of São Paulo and Minas Gerais, the leading Brazilian citrus production region, after 2015. The most recent common ancestor of viruses of the three lineages dates back to, at least, ∼1500 years ago. Since citrus plants were introduced in the Americas by the Portuguese around the 1520s, the Bayesian phylodynamic analysis suggested that the ancestors of the main CiLV-C lineages likely originated in contact with native vegetation of South America. The intensive expansion of CRD and SJP lineages in Brazil started probably linked to the beginning of the local citrus industry. The high prevalence of CiLV-C in the citrus belt of Brazil likely ensues from the intensive connectivity between orchards, which represents a potential risk toward pathogen saturation across the region.
Highlights
Brazil is the leading sweet orange producer in the world
Citrus orchard yields may be impacted by citrus leprosis (CL) disease, ranked first among the viral diseases affecting this crop in Brazil (Ramos-González et al, 2018)
The presence of citrus leprosis virus C (CiLV-C) was confirmed in all the 430 symptomatic samples collected from 304 plants of sweet orange, six of mandarin, and in other five citrus plants whose species could not be determined (Supplementary Table 1)
Summary
Brazil is the leading sweet orange producer in the world. Citrus orchard yields may be impacted by citrus leprosis (CL) disease, ranked first among the viral diseases affecting this crop in Brazil (Ramos-González et al, 2018). Control of CL reaches up to US$ 54 million/year, a value representing about 5% of the management cost of orchards in the main Brazilian citrus belt (Bassanezi et al, 2019). Despite the multi-etiological character of CL, citrus leprosis virus C (CiLV-C) is, by far, the prevalent causal agent in Brazil (Ramos-González et al, 2016, 2017, 2018; Chabi-Jesus et al, 2018). CiLV-C naturally infects Commelina benghalensis and Swinglea glutinosa and can be experimentally transmitted to plants of 28 families (León et al, 2008; Nunes et al, 2012; Garita et al, 2014; Arena et al, 2017)
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