Antagonism between salicylic acid and auxin responses directs root development during Tobamovirus infection

Abstract

Viral symptoms in plants are structural and physiological changes resulting from virus-induced manipulation of host pathways. While the effects of viruses on above-ground organs have been well-documented, their impact on the root system remains largely understudied. In tomato (Solanum lycopersicum), the emerging tomato brown rugose fruit virus (ToBRFV; Genus: Tobamovirus) causes significant reductions in root branching. However, the mechanisms underlying this symptom remained unexplored. Here, we provide evidence that tobamovirus-mediated suppression of root branching is conserved between ToBRFV and tomato mosaic virus (ToMV), with ToMV exhibiting a more severe effect over root development. Transcriptome analysis of tobamovirus-infected roots revealed a major shift from growth to defense, marked by the early activation of salicylic acid (SA) signaling. Conversely, auxin signaling was extensively reprogrammed; For example, auxin signaling suppressors such as Aux/IAAs were activated while expression of auxin response factors (ARFs), was downregulated. Importantly, SlARF19a showed reduced expression during infection. Functional analysis of Slarf19a mutants confirmed its critical role in root branching and the root’s developmental response to ToMV. We conclude that tobamovirus-mediated root suppression involves an inverse relationship between SA-mediated defense and auxin-mediated growth and identify SlARF19a as a key regulator in this developmental trade-off.