Abstract
Viruses have different strategies for infecting their hosts. Fast and acute infections result in the development of severe symptoms and may cause the death of the plant. By contrast, in a persistent interaction, the virus can survive within its host for a long time, inducing only mild symptoms. In this study, we investigated the gene expression changes induced in CymRSV-, crTMV-, and TCV-infected Nicotiana benthamiana and in PVX- and TMV-U1-infected Solanum lycopersicum plants after the systemic spread of the virus by two different high-throughput methods: microarray hybridization or RNA sequencing. Using these techniques, we were able to clearly differentiate between acute and persistent infections. We validated the gene expression changes of selected genes by Northern blot hybridization or by qRT-PCR. We show that, in contrast to persistent infections, the drastic shut-off of housekeeping genes, downregulation of photosynthesis-related transcripts and induction of stress genes are specific outcomes with acute infections. We also show that these changes are not a consequence of host necrosis or the presence of a viral silencing suppressor. Thermal imaging data and chlorophyll fluorescence measurements correlated very well with the molecular changes. We believe that the molecular and physiological changes detected during acute infections mostly contribute to virus symptom development. The observed characteristic physiological changes associated with economically more dangerous acute infections could serve as a basis for the elaboration of remote monitoring systems suitable for detecting developing virus infections in crops. Moreover, as molecular and physiological changes are characteristics of different types of virus lifestyles, this knowledge can support risk assessments of recently described novel viruses.
Highlights
High-throughput sequencing methods opened a new avenue for virus discovery [1]
The N. benthamiana plants were infected with Cymbidium ringspot virus (CymRSV), CymRSV19S, carnation Italian ringspot virus (CIRV), CIRV19S, crucifer-infecting tobacco mosaic virus (crTMV) and turnip crinkle virus (TCV)
N. benthamiana plants were infected with CymRSV (Tombusviruses, acute), crTMV (Tobamoviruses, acute) and TCV (Tombusviruses, persistent), whereas S. lycopersicum plants were infected with Potato virus X (PVX) (Potexviruses, acute) and tobacco mosaic virus U1 (TMV-U1) (Tobamoviruses, persistent)
Summary
High-throughput sequencing methods opened a new avenue for virus discovery [1]. more and more viruses are described each day, and assessing the importance and risk of these recently described viruses is very difficult. Gene expression studies in virus-infected plants usually investigate events at early timepoints after the infection, i.e., just after the virus has entered the host cell. At this early timepoint, host antiviral responses are activated, and the fate of the infection is determined. In an interaction with a susceptible plant, the virus gets past this barrier and advances into the stage of the infection, when it can move from cell to cell and long distances, colonising the whole plant During this process, other types of defence responses (such as antiviral RNA interference, RNAi) are activated [6]. With the availability of both host genomes and high-throughput methods such as microarray and RNA-sequencing (RNA-seq), an increasing number of studies investigate and characterize the molecular changes behind symptom development, usually in specific host-virus combinations [9,10,11,12,13,14,15,16,17,18,19,20]
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