TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation

Abstract

The susceptibility factor TOBAMOVIRUS MULTIPLICATION 1 (TOM1) is required for efficient multiplication of tobacco mosaic virus (TMV). Although some phylogenetic and functional analyses of the TOM1 family members have been conducted, a comprehensive analysis of the TOM1 homologues based on phylogeny from the most ancient to the youngest representatives within the plant kingdom, analysis of support for tobamovirus accumulation and interaction with other host and viral proteins has not been reported. In this study, using Nicotiana benthamiana and TMV as a model system, we functionally characterized the TOM1 homologues from N. benthamiana and other plant species from different plant lineages. We modified a multiplex genome editing tool and generated a sextuple mutant in which TMV multiplication was dramatically inhibited. We showed that TOM1 homologues from N. benthamiana exhibited variable capacities to support TMV multiplication. Evolutionary analysis revealed that the TOM1 family is restricted to the plant kingdom and probably originated in the Chlorophyta division, suggesting an ancient origin of the TOM1 family. We found that the TOM1 family acquired the ability to promote TMV multiplication after the divergence of moss and spikemoss. Moreover, the capacity of TOM1 orthologues from different plant species to promote TMV multiplication and the interactions between TOM1 and TOM2A and between TOM1 and TMV‐encoded replication proteins are highly conserved, suggesting a conserved nature of the TOM2A–TOM1–TMV Hel module in promoting TMV multiplication. Our study not only revealed a conserved nature of a gene module to promote tobamovirus multiplication, but also provides a valuable strategy for TMV‐resistant crop development.

Engineered Resistance to Tobamoviruses

“…It was found that using Crispr-Cas 9 to mutate all four gene family members had no apparent deleterious effects on plants but rendered them immune to TMV, ToMV and YoMV, while having no effect on susceptibility to infection by PVX or the Cucumovirus tomato aspermy virus [136]. TOM1 orthologs are conserved across a very broad taxonomic range of plants [143]. In addition to TOM1, TOM3 (another transmembrane protein that supports tobamovirus replication) and TOM2A (which plays a subsidiary role in supporting tobamovirus replication) have been identified among the factors supporting tobamovirus replication, using mutant screens.…”

Engineered Resistance to Tobamoviruses

“…It was found that using Crispr-Cas 9 to mutate all four gene family members had no apparent deleterious effects on plants but rendered them immune to TMV, ToMV and YoMV, while having no effect on susceptibility to infection by PVX or the Cucumovirus tomato aspermy virus [136]. TOM1 orthologs are conserved across a very broad taxonomic range of plants [143]. In addition to TOM1, mutant screens have identified other factors supporting tobamovirus replication including TOM3 (another transmembrane protein that supports tobamovirus replication) and TOM2A (which plays a subsidiary role in supporting tobamovirus replication).…”