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

P.B.E. Butterbach, M.G. Verlaan, A.M. Dullemans, H. Lohuis, R.G.F. Visser, Y. Bai, R.J.M. Kormelink

Research output: Contribution to journalArticleAcademicpeer-review

88 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)12942-12947
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number35
DOIs
Publication statusPublished - 2014

Keywords

  • short interfering rna
  • dna methylation
  • geminivirus al2
  • l2 proteins
  • adenosine kinase
  • gene
  • suppression
  • arabidopsis
  • plants
  • locus

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