A Survey on Plant Viruses in Natural Brassicaceae Communities Using RNA-Seq

Abstract

Studies on plant viruses are biased towards crop diseases and little is known about viruses in natural vegetation. We conducted extensive surveys of plant viruses in wild Brassicaceae plants occurring in three local plant communities in central Japan. We applied RNA-Seq with selective depletion of rRNA, which allowed us to detect infections of all genome-reported viruses simultaneously. Infections of Turnip mosaic virus (TuMV), Cucumber mosaic virus (CMV), Brassica yellows virus, Pelargonium zonate spot virus and Arabidopsis halleri partitivirus 1 were detected from the two perennial species, Arabidopsis halleri subsp. gemmifera and Rorippa indica. De novo assembly further detected partial sequences of a putative novel virus in Arabis fragellosa. Virus species composition and infection rate differed depending on site and plant species. Viruses were most frequently detected from the perennial clonal plant, A. halleri, in which a high clonal transmission rate of viruses across multiple years was confirmed. Phylogenetic analysis of TuMV and CMV showed that virus strains from wild Brassicaceae were included as a major clade of these viruses with other reported strains from crop plants, suggesting that viruses were shared among wild plants and crops. Our studies indicated that distribution of viruses in natural plant populations are determined by the combinations of life histories of viruses and hosts. Revealing viral distribution in the natural plant communities improves our knowledge on the ecology of plant viruses.

Seasonality of interactions between a plant virus and its host during persistent infection in a natural environment

“…The temperature dependence of TuMV spread within plants observed here was consistent with that in previous experimental studies [19]. On the other hand, lower leaves of winter rosettes functioned as a reservoir for the virus that subsequently transmitted to the clonal offspring of the host in spring, which resulted in high transmission rate (92%) as we reported previously [32]. Our study is the first to report seasonality in viral dynamics and virus-host interactions in naturally occurring infections of plant viruses.…”

“…However, TuMV is transmitted horizontally via aphids [74], and vertical transmission through seeds is rare [75,76]. In the TuMV ̶ A. halleri system, the effective transmission of virus through clonal propagation [32] is likely to provide a similar situation that favours low viral load to host plants as long as a single virus lineage utilises its own host for longer periods. Actually, it turned out that a single unique lineage of TuMV was able to persist for over a year in a single clonal lineage of host plants, being transmitted through clonal propagation of A. halleri.…”

“…gemmifera (A. halleri, hereafter), and Turnip mosaic virus (TuMV), a virus infecting it in natural environments. In a natural population of A. halleri in central Japan [30], we found that TuMV infections were common but without severe symptoms [31,32]. In our previous study, we applied RNA-Seq to simultaneously determine infection rate of all viruses and host responses in early summer, and found that 57% of examined plants were infected by TuMV, and a homologue of antiviral defence gene, ARGONAUTE 2 (AGO2), was upregulated in TuMVinfected plants [31].…”

“…In our previous study, we applied RNA-Seq to simultaneously determine infection rate of all viruses and host responses in early summer, and found that 57% of examined plants were infected by TuMV, and a homologue of antiviral defence gene, ARGONAUTE 2 (AGO2), was upregulated in TuMVinfected plants [31]. Arabidopsis halleri produces clonal rosettes, and we previously reported that TuMV was transmitted to 92% of clonal rosettes produced by TuMVinfected plants [32]. Due to the clonal rosette formation, A. halleri often forms plant patches that consist of multiple rosettes with a shared genotype.…”

Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation

“…Endogenous organisms might act as environmental factors that can result in divergent selection between populations. The TuMV infection rates were compared between multiple natural populations, and ranged from 0 to 57 % (Kamitani et al 2019). We still have limited knowledge on the regional variation in virus infection rates and whether this geographic variation is translated into differentiation among A. halleri populations.…”