Abstract

Tomato yellow leaf curl Sardinia virus (TYLCSV), a DNA virus belonging to the genus Begomovirus, causes severe losses in tomato crops. It infects only a limited number of cells in the vascular tissues, making difficult to detect changes in host gene expression linked to its presence. Here we present the first microarray study of transcriptional changes induced by the phloem-limited geminivirus TYLCSV infecting tomato, its natural host. The analysis was performed on the midrib of mature leaves, a material naturally enriched in vascular tissues. A total of 2206 genes were up-regulated and 1398 were down-regulated in infected plants, with an overrepresentation of genes involved in hormone metabolism and responses, nucleic acid metabolism, regulation of transcription, ubiquitin-proteasome pathway and autophagy among those up-regulated, and in primary and secondary metabolism, phosphorylation, transcription and methylation-dependent chromatin silencing among those down-regulated. Our analysis showed a series of responses, such as the induction of GA- and ABA-responsive genes, the activation of the autophagic process and the fine tuning of the plant immune system, observed only in TYLCSV-tomato compatible interaction so far. On the other hand, comparisons with transcriptional changes observed in other geminivirus-plant interactions highlighted common host responses consisting in the deregulation of biotic stress responsive genes, key enzymes in the ethylene biosynthesis and methylation cycle, components of the ubiquitin proteasome system and DNA polymerases II. The involvement of conserved miRNAs and of solanaceous- and tomato-specific miRNAs in geminivirus infection, investigated by integrating differential gene expression data with miRNA targeting data, is discussed.

Highlights

  • Geminiviruses are a large family of plant viruses able to infect a wide variety of plants worldwide

  • We hypothesized that viral effects on host gene expression would be more detectable in mature leaves, where developmental effects related to DNA replication and cell division are minimal

  • Comparing our list of DE genes with those obtained for South African cassava mosaic virus (SACMV)/Arabidopsis interaction, we found that the number of common DE genes was lower at 14 dpi (42 genes differentially expressed in both infections), intermediate at 24 dpi (103 DE genes in both infections) and higher at 36 dpi, with 166 genes differentially expressed in response to both viruses (78 of them were regulated in the same direction) (Fig.4A and Table S5)

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Summary

Introduction

Geminiviruses are a large family of plant viruses able to infect a wide variety of plants worldwide. The family is currently divided in seven genera, Becurtovirus, Begomovirus, Curtovirus, Eragrovirus, Mastrevirus,Topocuvirus and Turncurtovirus according to their genome organization, insect vector and host range [1,2]. All viruses belonging to these genera have a single-stranded circular DNA (ssDNA) genome and replicate in the nuclei of the host cells. The genus Begomovirus, with its more than 200 species, is the most represented. It includes viruses with either monopartite or bipartite genomes, transmitted by the whitefly Bemisia tabaci Genn., infecting a wide range of dicots in both the Old and the New World [3]

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