Dataset Information

Integrated single-base resolution maps of transcriptome, sRNAome and methylome of Tomato yellow leaf curl virus (TYLCV) in tomato.

ABSTRACT: Geminiviruses are plant ssDNA viruses that replicate through dsDNA intermediates and form minichromosomes which carry the same epigenetic marks as the host chromatin. During the infection, geminiviruses are targets of the post-transcriptional and transcriptional gene silencing machinery. To obtain insights into the connection between virus-derived small RNAs (vsRNAs), viral genome methylation and gene expression, we obtained the transcriptome, sRNAome and methylome from the geminivirus Tomato yellow leaf curl virus-infected tomato plants. The results showed accumulation of transcripts just at the viral ORFs, while vsRNAs spanned the entire genome, showing a prevalent accumulation at regions where the viral ORFs overlapped. The viral genome was not homogenously methylated showing two highly methylated regions located in the C1 ORF and around the intergenic region (IR). The compilation of those results showed a partial correlation between vsRNA accumulation, gene expression and DNA methylation. We could distinguish different epigenetic scenarios along the viral genome, suggesting that in addition to its function as a plant defence mechanism, DNA methylation could have a role in viral gene regulation. To our knowledge, this is the first report that shows integrative single-nucleotide maps of DNA methylation, vsRNA accumulation and gene expression from a plant virus.

SUBMITTER: Piedra-Aguilera A

PROVIDER: S-EPMC6393547 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Integrated single-base resolution maps of transcriptome, sRNAome and methylome of Tomato yellow leaf curl virus (TYLCV) in tomato.

Piedra-Aguilera Álvaro Á Jiao Chen C Luna Ana P AP Villanueva Francisco F Dabad Marc M Esteve-Codina Anna A Díaz-Pendón Juan A JA Fei Zhangjun Z Bejarano Eduardo R ER Castillo Araceli G AG

Scientific reports 20190227 1

Geminiviruses are plant ssDNA viruses that replicate through dsDNA intermediates and form minichromosomes which carry the same epigenetic marks as the host chromatin. During the infection, geminiviruses are targets of the post-transcriptional and transcriptional gene silencing machinery. To obtain insights into the connection between virus-derived small RNAs (vsRNAs), viral genome methylation and gene expression, we obtained the transcriptome, sRNAome and methylome from the geminivirus Tomato ye ...[more]

PMID: 30814535

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Project description:Herbivory defense systems in plants are largely regulated by jasmonate-(JA) and salicylate-(SA) signaling pathways. Such defense mechanisms may impact insect feeding dynamic, may also affect the transmission-acquisition relationship among virus, plants and vectoring insects. In the context of the tomato - whitefly - Tomato Yellow Leaf Curl Virus (TYLCV) biological model, we tested the impact of pre-infesting plants with a non-vector insect (aphid Myzus persicae) on feeding dynamics of a vector insect (whitefly Bemisia tabaci) as well as virus transmission-acquisition. We showed that an aphid herbivory period of 0-48 h led to a transient systemic increase of virus concentration in the host plant (root, stem, and leaf), with the same pattern observed in whiteflies feeding on aphid-infested plants. We used real-time quantitative PCR to study the expression of key genes of the SA- and JA-signaling pathways, as well as electrical penetration graph (EPG) to characterize the impact of aphid pre-infestation on whitefly feeding during TYLCV transmission (whitefly to tomato) and acquisition (tomato to whitefly). The impact of the duration of aphid pre-infestation (0, 24, or 48 h) on phloem feeding by whitefly (E2) during the transmission phase was similar to that of global whitefly feeding behavior (E1, E2 and probing duration) during the acquisition phase. In addition, we observed that a longer phase of aphid pre-infestation prior to virus transmission by whitefly led to the up-regulation and down-regulation of SA- and JA-signaling pathway genes, respectively. These results demonstrated a significant impact of aphid pre-infestation on the tomato - whitefly - TYLCV system. Transmission and acquisition of TYLCV was positively correlated with feeding activity of B. tabaci, and both were mediated by the SA- and JA-pathways. TYLCV concentration during the transmission phases was modulated by up- and down-regulation of SA- and JA-pathways, respectively. The two pathways were inconsistent during the acquisition phase; SA- related genes were up-regulated, whereas those up- and down-stream of the JA pathway showed a more complex relationship. These findings enhance our understanding of plant - herbivore - virus interactions, which are potentially important for development of ecologically sound pest and pathogen management programs.

Project description:BackgroundTomato yellow leaf curl virus (TYLCV), a monopartite begomovirus (family Geminiviridae) is responsible for heavy yield losses for tomato production around the globe. In Oman at least five distinct begomoviruses cause disease in tomato, including TYLCV. Unusually, TYLCV infections in Oman are sometimes associated with a betasatellite (Tomato leaf curl betasatellite [ToLCB]; a symptom modulating satellite). RNA interference (RNAi) can be used to develop resistance against begomoviruses at either the transcriptional or post-transcriptional levels.ResultsA hairpin RNAi (hpRNAi) construct to express double-stranded RNA homologous to sequences of the intergenic region, coat protein gene, V2 gene and replication-associated gene of Tomato yellow leaf curl virus-Oman (TYLCV-OM) was produced. Initially, transient expression of the hpRNAi construct at the site of virus inoculation was shown to reduce the number of plants developing symptoms when inoculated with either TYLCV-OM or TYLCV-OM with ToLCB-OM to Nicotiana benthamiana or tomato. Solanum lycopersicum L. cv. Pusa Ruby was transformed with the hpRNAi construct and nine confirmed transgenic lines were obtained and challenged with TYLCV-OM and ToLCB-OM by Agrobacterium-mediated inoculation. For all but one line, for which all plants remained symptomless, inoculation with TYLCV-OM led to a proportion (≤25%) of tomato plants developing symptoms of infection. For inoculation with TYLCV-OM and ToLCB-OM all lines showed a proportion of plants (≤45%) symptomatic. However, for all infected transgenic plants the symptoms were milder and virus titre in plants was lower than in infected non-transgenic tomato plants.ConclusionsThese results show that RNAi can be used to develop resistance against geminiviruses in tomato. The resistance in this case is not immunity but does reduce the severity of infections and virus titer. Also, the betasatellite may compromise resistance, increasing the proportion of plants which ultimately show symptoms.

Dataset Information

Integrated single-base resolution maps of transcriptome, sRNAome and methylome of Tomato yellow leaf curl virus (TYLCV) in tomato.

Publications

Integrated single-base resolution maps of transcriptome, sRNAome and methylome of Tomato yellow leaf curl virus (TYLCV) in tomato.

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