Ty‐1, a universal resistance gene against geminiviruses that is compromised by co‐replication of a betasatellite

Abstract

Tomato yellow leaf curl virus (TYLCV), a begomovirus, causes large yield losses and breeding for resistance is an effective way to combat this viral disease. The resistance gene Ty-1 codes for an RNA-dependent RNA polymerase and has recently been shown to enhance transcriptional gene silencing of TYLCV. Whereas Ty-1 was earlier shown to also confer resistance to a bipartite begomovirus, here it is shown that Ty-1 is probably generic to all geminiviruses. A tomato Ty-1 introgression line, but also stable transformants of susceptible tomato cv. Moneymaker and Nicotiana benthamiana (N. benthamiana) expressing the Ty-1 gene, exhibited resistance to begomoviruses as well as to the distinct, leafhopper-transmitted beet curly top virus, a curtovirus. Stable Ty-1 transformants of N. benthamiana and tomato showed fewer symptoms and reduced viral titres on infection compared to wild-type plants. TYLCV infections in wild-type N. benthamiana plants in the additional presence of a betasatellite led to increased symptom severity and a consistent, slightly lowered virus titre relative to the high averaged levels seen in the absence of the betasatellite. On the contrary, in Ty-1 transformed N. benthamiana viral titres increased in the presence of the betasatellite. The same was observed when these Ty-1-encoding plants were challenged with TYLCV and a potato virus X construct expressing the RNA interference suppressor protein βC1 encoded by the betasatellite. The resistance spectrum of Ty-1 and the durability of the resistance are discussed in light of antiviral RNA interference and viral counter defence strategies.

The Global Dimension of Tomato Yellow Leaf Curl Disease: Current Status and Breeding Perspectives

“…Usually the resulting new disease complexes are characterized by more severe symptoms consisting of extremely stunted and distorted plants ( Figure 4 ) [ 33 , 55 ]. In N. benthamiana , co-replication of TYLCV with ageratum yellow vein betasatellite (AYVB) increases the symptom severity level [ 56 , 57 ]. Co-infection of TYLCMLV and cotton leaf curl Gezira betallatellite (CLCuGB) by cross-feeding of whiteflies resulted in more severe symptoms [ 33 , 54 ].…”

“…Ty-1 confers resistance to TYLCV based on enhanced TGS by increasing cytosine methylation of the viral genome [ 81 ]. Ty-1 -mediated antiviral TGS response has been considered to be generic against geminiviruses as Ty-1 was shown to also confer resistance to a bipartite begomovirus tomato severe rugose virus (ToSRV) [ 81 ] and the leafhopper-transmitted beet curly top virus (BCTV), a curtovirus [ 57 ]. However, co-inoculation with betasatellites expressing the βC1 protein compromises Ty-1 -mediated resistance and induces disease symptoms [ 57 ].…”

Metagenomics of Neotropical Single-Stranded DNA Viruses in Tomato Cultivars with and without the Ty-1 Gene

“…Therefore, the Ty -1 gene is representing an entirely new class of disease resistance/tolerance genes that operates by intensifying the levels of transcriptional silencing of viral genes. More recent studies have shown that the Ty -1 gene can also confer resistance to Beet curly top virus (a viral species of the genus Curtovirus ) in genetically transformed Nicotiana benthamiana plants [ 34 ]. However, no information is yet available about the effects of the Ty -1 gene on ssDNA viruses and subviral agents described in association with tomatoes in neotropical areas.…”

Secondary siRNAs in Plants: Biosynthesis, Various Functions, and Applications in Virology

“…RDR3 from Salvia miltiorrhiza was induced after cucumber mosaic virus (CMV) infection, suggesting its role in the antiviral silencing ( Shao and Lu, 2014 ). Tomato Ty1/Ty3 genes encode for RDRγ and are associated with antiviral resistance ( Voorburg et al, 2020 ). Tomato cultivars with Ty1/Ty3 displayed resistance against begomovirus and tomato yellow leaf curl virus and displayed enhanced viral siRNA (VsiRNA) generation and cytosine methylation of the begomovirus genome.…”