Comparative Transcriptome Analysis Provides Molecular Insights into the Interaction of Beet necrotic yellow vein virus and Beet soil-borne mosaic virus with Their Host Sugar Beet

Abstract

Beet necrotic yellow vein virus (BNYVV) and Beet soil-borne mosaic virus (BSBMV) are closely related species, but disease development induced in their host sugar beet displays striking differences. Beet necrotic yellow vein virus induces excessive lateral root (LR) formation, whereas BSBMV-infected roots appear asymptomatic. A comparative transcriptome analysis was performed to elucidate transcriptomic changes associated with disease development. Many differentially expressed genes (DEGs) were specific either to BNYVV or BSBMV, although both viruses shared a high number of DEGs. Auxin biosynthesis pathways displayed a stronger activation by BNYVV compared to BSBMV-infected plants. Several genes regulated by auxin signalling and required for LR formation were exclusively altered by BNYVV. Both viruses reprogrammed the transcriptional network, but a large number of transcription factors involved in plant defence were upregulated in BNYVV-infected plants. A strong activation of pathogenesis-related proteins by both viruses suggests a salicylic acid or jasmonic acid mediated-defence response, but the data also indicate that both viruses counteract the SA-mediated defence. The ethylene signal transduction pathway was strongly downregulated which probably increases the susceptibility of sugar beet to Benyvirus infection. Our study provides a deeper insight into the interaction of BNYVV and BSBMV with the economically important crop sugar beet.

Genome-Wide microRNA Profiling Using Oligonucleotide Microarray Reveals Regulatory Networks of microRNAs in Nicotiana benthamiana During Beet Necrotic Yellow Vein Virus Infection

“…Our findings revealed that BNYVV infection induced ethylene biosynthesis but repressed GA signal pathway in the infected N. benthamiana leaves, consistent with the results from transcriptome analysis of BNYVV-infected N. benthamiana leaves reported previously [10]. However, Fernando Gil et al reported that the ethylene signal transduction pathway is strongly suppressed in the BNYVV-infected root tissues of sugar beet [11], and neither B. macrocarpa nor B. vulgaris was reported to show changes in the genes of the GA signal pathway during BNYVV-infection [7,11,12]. Instead, the auxin response is predominantly regulated in both B. macrocarpa and B. vulgaris during BNYVV infection [7,11,12], suggesting plant-species-specific hormonal responses to BNYVV.…”

“…However, Fernando Gil et al reported that the ethylene signal transduction pathway is strongly suppressed in the BNYVV-infected root tissues of sugar beet [11], and neither B. macrocarpa nor B. vulgaris was reported to show changes in the genes of the GA signal pathway during BNYVV-infection [7,11,12]. Instead, the auxin response is predominantly regulated in both B. macrocarpa and B. vulgaris during BNYVV infection [7,11,12], suggesting plant-species-specific hormonal responses to BNYVV. Notably, auxin increased considerably in sugar beet roots after BNYVV infection [11,12], whereas in the leaves of B. macrocarpa, the auxin response seems to be repressed, as evidenced by the upregulations of miR393 and consequent down-regulation of transport inhibitor response protein 1 [7].…”

“…A study extended this research by conducting transcriptomic analysis of naturally infected sugar beet (Beta vulgaris) roots [11]. A comparison of these studies revealed that some signaling pathways, such as the pathogenesis-related defense, cell-wall-associated, and hormone biosynthesis, are regulated in all of these different hosts [8,[10][11][12], suggesting evolutionarily conserved responses of plants to BNYVV infection. However, some genes showed diverse expression patterns in different tissues across the experimental and natural hosts.…”

“…We characterized the transcriptome of N. benthamiana and B. macrocarpa leaves in response to BNYVV infection, using the deep sequencing previously reported [8,10]. A study extended this research by conducting transcriptomic analysis of naturally infected sugar beet (Beta vulgaris) roots [11]. A comparison of these studies revealed that some signaling pathways, such as the pathogenesis-related defense, cell-wall-associated, and hormone biosynthesis, are regulated in all of these different hosts [8,[10][11][12], suggesting evolutionarily conserved responses of plants to BNYVV infection.…”

“…However, some genes showed diverse expression patterns in different tissues across the experimental and natural hosts. For example, expansin-related genes were up-regulated in the leaves of B. macrocarpa and the root of B. vulgaris [8,11,12], but were repressed in the BNYVV-infected N. benthamiana leaves [10], suggesting that the gene expression in response to BNYVV infection is tissue-dependent and also varies among distantly related plant species.…”