title: A nuclear-replicating viroid antagonizes infectivity and accumulation of a geminivirus by upregulating methylation-related genes and inducing hypermethylation of viral DNA.
abstract: DNA methylation and post-transcriptional gene silencing play critical roles in controlling infection of single-stranded (ss) DNA geminiviruses and ssRNA viroids, respectively, but both pathogens can counteract these host defense mechanisms and promote their infectivity. Moreover, a specific role of DNA methylation in viroid-host interactions is not yet confirmed. Here, using an experimental system where two nuclear-replicating agents, the geminivirus tomato yellow leaf curl Sardinia virus (TYLCSV) and potato spindle tuber viroid (PSTVd), co-infect their common host tomato, we observed that PSTVd severely interferes with TYLCSV infectivity and accumulation, most likely as a consequence of strong activation of host DNA methylation pathways. In fact, PSTVd alone or in co-infection with TYLCSV significantly upregulates the expression of key genes governing DNA methylation in plants. Using methylation-sensitive restriction and bisulfite conversion assays, we further showed that PSTVd infection promotes a strong hypermethylation of TYLCSV DNA, thus supporting a mechanistic link with the antagonism of the viroid on the virus in co-infected tomato plants. These results describe the interaction between two nuclear-replicating pathogens and show that they differentially interfere with DNA methylation pathways.
authors.affiliation: Institute for Sustainable Plant Protection, National Research Council of Italy, Bari, 70126, Italy.
authors.forename: Enza Maria
authors.initials: EM
authors.lastname: Torchetti
authors.affiliation: Institute for Sustainable Plant Protection, National Research Council of Italy, Torino, 10135, Italy.
authors.forename: Mattia
authors.initials: M
authors.lastname: Pegoraro
authors.affiliation: Institute for Sustainable Plant Protection, National Research Council of Italy, Bari, 70126, Italy.
authors.forename: Beatriz
authors.initials: B
authors.lastname: Navarro
authors.affiliation: The Sainsbury Laboratory, University of Cambridge, Cambridge, CB2 1LR, United Kingdom.
authors.forename: Marco
authors.initials: M
authors.lastname: Catoni
authors.affiliation: Institute for Sustainable Plant Protection, National Research Council of Italy, Bari, 70126, Italy.
authors.forename: Francesco
authors.initials: F
authors.lastname: Di Serio
authors.affiliation: Institute for Sustainable Plant Protection, National Research Council of Italy, Torino, 10135, Italy.
authors.forename: Emanuela
authors.initials: E
authors.lastname: Noris
mesh_terms: D002467:Cell Nucleus / Q000821:virology*; D019175:DNA Methylation; D004261:DNA Replication; D004279:DNA, Viral / Q000096:biosynthesis*; D017791:Geminiviridae / Q000254:growth & development*; D018551:Solanum lycopersicum / Q000821:virology; D014762:Viral Interference; D014772:Viroids / Q000254:growth & development*
chemical_list: D004279:DNA, Viral