Global Advances in Tomato Virome Research: Current Status and the Impact of High-Throughput Sequencing

Abstract

Viruses cause a big fraction of economically important diseases in major crops, including tomato. In the past decade (2011-2020), many emerging or re-emerging tomato-infecting viruses were reported worldwide. In this period, 45 novel viral species were identified in tomato, 14 of which were discovered using high-throughput sequencing (HTS). In this review, we first discuss the role of HTS in these discoveries and its general impact on tomato virome research. We observed that the rate of tomato virus discovery is accelerating in the past few years due to the use of HTS. However, the extent of the post-discovery characterization of viruses is lagging behind and is greater for economically devastating viruses, such as the recently emerged tomato brown rugose fruit virus. Moreover, many known viruses still cause significant economic damages to tomato production. The review of databases and literature revealed at least 312 virus, satellite virus, or viroid species (in 22 families and 39 genera) associated with tomato, which is likely the highest number recorded for any plant. Among those, here, we summarize the current knowledge on the biology, global distribution, and epidemiology of the most important species. Increasing knowledge on tomato virome and employment of HTS to also study viromes of surrounding wild plants and environmental samples are bringing new insights into the understanding of epidemiology and ecology of tomato-infecting viruses and can, in the future, facilitate virus disease forecasting and prevention of virus disease outbreaks in tomato.

Keywords: high-throughput sequencing; metagenomics; tomato; virome; virus discovery; virus diversity; virus ecology; virus epidemiology.

FIGURE 1

Global distribution of virus species newly discovered in the 2011 to 2020 period. Abbreviated virus names (see Table 1) are shown in groups corresponding to the ecozones in which they were discovered (Antarctic is not shown, for simplicity, China and Indonesia are included in Indo-Malay, and Mexico is included in the Neotropic ecoregion) (A). In the map (B), ecoregions are delimited by gray lines and countries colored in orange are top producers of tomato in the 2008–2018 period, recording at least 8.14 million tons of total tomato produced (FAOSTAT, 2020). Viruses detected in more than one ecozone are shown on the map as number-coded yellow circles (1–4) corresponding to the virus species designated in the list in (A). The numbers of annual new tomato virus discoveries in the 2011–2020 period are shown in (C) and the numbers of new tomato virus discoveries per ecoregion in this time period are shown in (D). The map was created using www.mapchart.net under the CC BY-SA 4.0 license.

FIGURE 2

Post-discovery characterization of new tomato-infecting viruses according to the literature review. Percentages of newly discovered virus species fulfilling each of the 14 characterization criteria are shown for viruses discovered by HTS or other methods (A). Fulfillment of characterization criteria plotted through the years elapsed since the first report is shown as a line plot (B), wherein each line represents a single virus and the evolution of its characterization; the lines corresponding to the emerging tomato brown rugose fruit virus (ToBRFV), and the first two tomato viruses discovered through HTS, tomato mottle mosaic virus (ToMMV) and tomato necrotic stunt virus (ToNStV), are labeled.

FIGURE 3

Taxonomic distribution of virus and viroid species that were reported to infect or were associated with tomato. The green horizontal bar represents tomato viruses discovered before 2011 and within the 2011–2020 period. Known species reported before 2011 (including all known viruses that were first associated in tomato within the 2011–2020 period) are shown in the dark green portion on the left and extended in pie chart callout, where their distribution across viral families is shown. Species newly discovered in 2011–2020 are shown in the light green portion of the bar and extended in bar chart callout, where their distribution across viral families is shown. In both callouts, families of DNA viruses, RNA viruses, and viroids are designated with differently hatched backgrounds.