Genetic variability in the 3′UTR RNA1 of tomato torrado virus: Implications for virus transmission by whitefly (Trialeurodes vaporariorum)

Tomato torrado virus (ToTV) is a whitefly-transmitted pathogen causing tomato necrosis. ToTV's genome consists of two positive single-stranded RNAs, with significant variability observed in RNA1. This study verified the hypothesis that deletions in the 3′untranslated region (UTR) of RNA1 affect virus acquisition and its spreading to healthy plants. We found that ToTV-Kra (wild-type RNA1, referred to as var1) as well as its shortened variants, with different length deletions in 3′UTR RNA1 (referred to as var2Δ6, var3Δ49, var4Δ44, and var5Δ163), along with wild-type RNA2 were acquired and spread by Trialeurodes vaporariorum, leading to necrosis in tomatoes. Analysis of the RNA1 and RNA2 quantities detected in stylets revealed that, in most variants, RNA2 was more abundant than RNA1. The highest viral RNA levels (RNA1 and 2) and the most efficient transmission were observed for the longest ToTV-Kra variants (var1, var2Δ6), whereas var5Δ163, the shortest variant along with the longest one exhibited a higher RNA1 titer in insect stylets. Overall, the longest RNA1 variant enabled the most efficient virus uptake from source plants.

While the mechanisms underlying the emergence of deletion variants remain unexplored, notable differences exist in viral load in whiteflies and subsequent replication in plants. On this basis, we assumed that 3′UTR variability may be an evolutionary adaptation of ToTV to transmission mode.