Selective modification of rice (Oryza sativa) gene expression by rice stripe virus infection

Abstract

Rice stripe disease, caused by rice stripe virus (RSV), is one of the major virus diseases in east Asia. Rice plants infected with RSV usually show symptoms such as chlorosis, weakness, necrosis in newly emerged leaves and stunting. To reveal rice cellular systems influenced by RSV infection, temporal changes in the transcriptome of RSV-infected plants were monitored by a customized rice oligoarray system. The transcriptome changes in RSV-infected plants indicated that protein-synthesis machineries and energy production in the mitochondrion were activated by RSV infection, whereas energy production in the chloroplast and synthesis of cell-structure components were suppressed. The transcription of genes related to host-defence systems under hormone signals and those for gene silencing were not activated at the early infection phase. Together with concurrent observation of virus concentration and symptom development, such transcriptome changes in RSV-infected plants suggest that different sets of various host genes are regulated depending on the development of disease symptoms and the accumulation of RSV. INTRODUCTIONRice stripe disease is the most severe virus disease of rice in east Asia. Typical symptoms are chlorosis and weakness on newly emerged leaves. The plant becomes considerably stunted when affected at the early growth stages (Ou, 1972). Rice stripe disease also causes necrosis of newly emerged leaves (Takahashi et al., 1991). The causal virus is Rice stripe virus (RSV), which belongs to the genus Tenuivirus (Falk & Tsai, 1998). RSV is transmitted by small brown planthopper (SBPH; Laodelphax striatellus), Terthron albovittatum, Unkanodes sapporonus and Unkanodes albifascia (Falk & Tsai, 1998;Ou, 1972). RSV has a thin, filamentous shape and no envelope. The genome consists of four single-stranded RNA segments; RNA1 is negative-sense and RNAs 2-4 are ambisense. Viral mRNAs transcribed from viral RNA or viral cRNA by RNA-dependent RNA polymerase are released to the cytoplasm. Subsequently, a 59-capped short ribonucleotide leader cleaved from the host mRNA is added to the viral mRNAs by cap-snatching. The 59-capped RSV RNA is transcribed efficiently in host cells (Falk & Tsai, 1998;Shimizu et al., 1996). Genes encoding a gene-silencing suppressor and movement proteins were also identified in the RSV genome (Lu et al., 2009;Xiong et al., 2008Xiong et al., , 2009. Although extensive functional analysis of the RSV genome has been conducted, there have been no reports on the interaction between RSV and rice plants, which may clarify the mechanisms behind the appearance of disease symptoms.Rice is a model cereal plant, for which many genomic and transcriptome resources and tools are already available (Liang et al., 2008;Ouyang et al., 2007; Rice Annotation Project, 2008; Rice Full-length cDNA Consortium, 2003). The elucidation of genome sequences and structures in diverse organisms has led to the development of various high-throughput genome and transcriptome analytical tools. Numerous transcriptome profiles in...

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

“…3A). It has been reported that RSV infection induced the expression of OsRDR1 in rice (Satoh et al, 2010;Du et al, 2011). As we have shown that RSV infection induced the accumulation of miR444 (Fig.…”

“…The expression of the key factors of RNA-silencing pathways usually is activated by virus infection at the transcriptional level to increase the activities of antiviral RNA silencing. For example, the expression of AGO1, AGO2, or RDR1 was usually induced by infection with diverse viruses (Yang et al, 2004;Alamillo et al, 2006;Zhang et al, 2006;Azevedo et al, 2010;He et al, 2010;Satoh et al, 2010;Várallyay et al, 2010;Du et al, 2011;Harvey et al, 2011). However, the molecular mechanisms of activation of the expression of these antiviral genes are unknown.…”

“…RDR1 orthologs have been reported to be virus or salicylic acid inducible in different plants, including Arabidopsis, Nicotiana spp., Medicago truncatula, maize (Zea mays), and rice (Oryza sativa; Yang et al, 2004;Alamillo et al, 2006;He et al, 2010;Satoh et al, 2010;Du et al, 2011), and to provide basal resistance to several viruses by participating in the biogenesis of virusderived secondary siRNAs (Diaz-Pendon et al, 2007;Qi et al, 2009;Garcia-Ruiz et al, 2010;Wang et al, 2010). Recently, it was reported that RDR1 also is responsible for the production of a distinct class of virus-activated siRNAs, which direct widespread silencing of host genes to confer broad-spectrum antiviral activity in Arabidopsis (Cao et al, 2014), indicating that RDR1 plays a key role in antiviral resistance by silencing both the viral RNAs and the host immunity-related genes.…”

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?

“…However, unlike other known dicot antiviral responses, we found ;30 protein kinases, particularly those in the receptor-like kinase subfamily, which are uniquely altered in both PMV and PMV+SPMV triggered responses in Brachypodium (Mandadi and Scholthof, 2012). This overrepresentation of protein kinases appears to be a unique feature of monocots, as our transcriptome comparisons with the few other reported monocot virus infections, such as maize infected with Rice black-streaked dwarf virus (genus Phytoreovirus) (Jia et al, 2012) and rice infected with Rice stripe virus (genus Tenuivirus) (Satoh et al, 2010), also revealed a higher proportion of upregulated kinases in the respective monocot virus infections. Together, these results suggest that although monocot and dicot plants share some commonalities, they have discrete and unique responses to plant virus infections.…”

Inducible transgenic tobacco system to study the mechanisms underlying chlorosis mediated by the silencing of chloroplast heat shock protein 90

“…Rice stripe virus (RSV) downregulates CPRGs during infection and disturbs the photosynthesis [23]. The perturbation of photosynthesis by RSV might be caused by the regulation of a special set of miRNAs that target key genes in chloroplast zeaxanthin cycle, which can lead to impaired chloroplast structure and function [35].…”