Tomato yellow leaf curl virus resistance by Ty-1 involves increased cytosine methylation of viral genomes and is compromised by cucumber mosaic virus infection

Abstract

Tomato yellow leaf curl virus (TYLCV) and related begomoviruses are a major threat to tomato production worldwide and, to protect against these viruses, resistance genes from different wild tomato species are introgressed. Recently, the Ty-1 resistance gene was identified, shown to code for an RNA-dependent RNA polymerase and to be allelic with Ty-3. Here we show that upon TYLCV challenging of resistant lines carrying Ty-1 or Ty-3, low virus titers were detected concomitant with the production of relatively high levels of siRNAs whereas, in contrast, susceptible tomato Moneymaker (MM) revealed higher virus titers but lower amounts of siRNAs. Comparative analysis of the spatial genomic siRNA distribution showed a consistent and subtle enrichment for siRNAs derived from the V1 and C3 genes in Ty-1 and Ty-3. In plants containing Ty-2 resistance the virus was hardly detectable, but the siRNA profile resembled the one observed in TYLCV-challenged susceptible tomato (MM). Furthermore, a relative hypermethylation of the TYLCV V1 promoter region was observed in genomic DNA collected from Ty-1 compared with that from (MM). The resistance conferred by Ty-1 was also effective against the bipartite tomato severe rugose begomovirus, where a similar genome hypermethylation of the V1 promoter region was discerned. However, a mixed infection of TYLCV with cucumber mosaic virus compromised the resistance. The results indicate that Ty-1 confers resistance to geminiviruses by increasing cytosine methylation of viral genomes, suggestive of enhanced transcriptional gene silencing. The mechanism of resistance and its durability toward geminiviruses under natural field conditions is discussed.RNAi | Solanaceae T omato yellow leaf curl virus disease causes enormous yield losses in tomato production worldwide and is caused by different related begomoviruses, with tomato yellow leaf curl virus (TYLCV) as the most important one. The virus, like all begomoviruses, is transmitted in a persistent manner by the whitefly Bemisia tabaci. TYLCV contains a monopartite single-stranded DNA genome that is bidirectionally transcribed for the expression of six partially overlapping ORFs. The genes responsible and involved in the regulation of genome replication and transcription (C1-C4) locate to the left-hand side of the genome, whereas those involved in packaging, movement, and transmission (V1 and V2) are located on the right-hand side. Of the genes involved in replication, the replication-associated protein (C1), transcription activator protein (C2), and replication enhancer protein (C3) have been relatively well studied and described. The right hand-side genes code for the coat protein (CP; V1) and precoat protein (V2). Because geminiviruses do not code for their own DNA polymerase, they reactivate the S phase in differentiated cells to support and enable replication of their DNA genome (1).Besides control of insect vector populations, breeding for resistance against TYLCV has been deployed as the main strategy in disease management. Currently, s...

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

“…The first line of defense is posttranscriptional gene silencing (PTGS)-mediated RNA interference (RNAi) that can aggressively decrease geminivirus transcripts (4,16,17,19,21). RNAdependent DNA methylation (RdDM)-mediated TGS also functions as a defense mechanism against geminivirus chromatin (5,(22)(23)(24). Recently, R gene-mediated resistance has been proposed as another essential defense strategy against geminiviruses.…”

Resistance-Gene-Mediated Defense Responses against Biotic Stresses in the Crop Model Plant Tomato

“…Ty-1 and Ty-3, both derived from Solanum chilense and are allelic. The Ty-1/Ty-3-mediated defense against TYLCV is somehow different from tomato defense against other viruses as TYLCV shows low levels of viral replication and systemic spread but with moderate (as with Ty-3) or no (as with Ty-1) visual symptoms [108]. Ty-1 and Ty-3 are allelic and represents a unique category of R-genes that encode for RNA-dependent RNA polymerases (RdRp) unlike most of the R-genes discussed so far that belongs to NLR family.…”

“…Ty-1 and Ty-3 are allelic and represents a unique category of R-genes that encode for RNA-dependent RNA polymerases (RdRp) unlike most of the R-genes discussed so far that belongs to NLR family. Ty-1 and Ty-3 are proposed to confer resistance to TYLCV by amplifying the RNAi signal [108]. The catalytic domain of the Ty-1/Ty-3 allele is characterized by a five-amino acid motif, DFDGD [108].…”

“…Ty-1 and Ty-3 are proposed to confer resistance to TYLCV by amplifying the RNAi signal [108]. The catalytic domain of the Ty-1/Ty-3 allele is characterized by a five-amino acid motif, DFDGD [108]. As compared to susceptible tomato plants, Ty-1/Ty-3 plants have higher levels of siRNA amplifications and Ty-1 plants also show higher levels of TYLCV DNA methylation [109].…”

Emerging threats of begomoviruses to the cultivation of medicinal and aromatic crops and their management strategies

“…Although transcriptional gene silencing confers resistance in wild tomatoes and this could be genetically engineered in other plants. Ty resistance gene is responsible for this TGS phenomenon [27]. Combination of Ty (Ty-1, and Ty2, Ty3, Ty4 and Ty5) gene has been reported in wild tomato to provide high level of resistance against Tomato yellow leaf curl virus (TYLCV).…”