Abstract

A complex of begomoviruses (Geminiviridae) can cause severe tomato yield losses in the neotropics. Here, next-generation sequencing was employed for large-scale assessment of single-stranded (ss)DNA virus diversity in tomatoes either harboring or lacking the large-spectrum begomovirus tolerance Ty-1 gene. Individual leaf samples exhibiting begomovirus-like symptoms (n = 107) were field-collected, circular DNA-enriched, subdivided into pools (with and without Ty-1), and Illumina-sequenced. Virus-specific PCR and Sanger dideoxy sequencing validations confirmed 15 distinct ssDNA virus/subviral agents (occurring mainly in mixed infections), which highlight the potential drawbacks of employing virus-specific resistance in tomato breeding. More viruses (14 versus 6 species) were observed in tomatoes without the Ty-1 gene. A gemycircularvirus (Genomoviridae), a new alpha-satellite, and two novel Begomovirus species were identified exclusively in samples without the Ty-1 gene. A novel begomovirus was found only in the Ty-1 pool, being the only species associated with severe symptoms in Ty-1 plants in our survey. Our work is the first step towards the elucidation of the potential begomovirus adaptation to Ty-1 and its specific filtering effects on a subset of ssDNA viral/subviral agents.

Highlights

  • Geminiviridae is the largest family of plant-infecting viruses, and is currently organized into nine genera: Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus, and Turncurtovirus [1]

  • The results reported here provide useful information about the population dynamics of begomoviruses associated with tomato crops across three major tomato-producing regions of central

  • Our work is in agreement with the notion that Next-generation sequencing (NGS) is a powerful strategy to identify known viruses and novel viruses and subviral agents

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Summary

Introduction

Geminiviridae is the largest family of plant-infecting viruses, and is currently organized into nine genera: Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus, and Turncurtovirus [1]. The classification at the genus level is based upon host range, the associated insect vector(s), genomic organization, and phylogenetic relationships [1,2,3]. In 2016, two novel viral families with non-enveloped, circular, single-stranded DNA (ssDNA) genomes with sizes ranging from 2.0 to 2.4 kb were created and named as Pleolipoviridae and Genomoviridae. The Genomoviridae family comprises nine genera: Gemycircularvirus, Gemyduguivirus, Gemygorvirus, Gemykibivirus, Gemykolovirus, Gemykrogvirus, Gemykroznavirus, Gemytondvirus, and Gemyvongvirus [1]. The genus Begomovirus is composed of whitefly-transmitted species with one (=monopartite) or two (=bipartite) circular, ssDNA genomic component(s) with ≈2.6 kb that are encapsidated separately into twinned particles formed by two incomplete icosahedrons [2,4]. The begomovirus transmission is characterized as being non-propagative and circulative, and is carried out by members

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