Transcriptomic profiling reveals the complex interaction between a bipartite begomovirus and a cucurbitaceous host plant

Abstract

Background: Begomoviruses are major constraint in the production of many crops. Upon infection, begomoviruses may substantially modulate plant biological processes. While how monopartite begomoviruses interact with their plant hosts has been investigated extensively, bipartite begomoviruses-plant interactions are understudied. Moreover, as one of the major groups of hosts, cucurbitaceous plants have been seldom examined in the interaction with begomoviruses.

Results: We profiled the zucchini transcriptomic changes induced by a bipartite begomovirus squash leaf curl China virus (SLCCNV). We identified 2275 differentially-expressed genes (DEGs), of which 1310 were upregulated and 965 were downregulated. KEGG enrichment analysis of the DEGs revealed that many pathways related to primary and secondary metabolisms were enriched. qRT-PCR verified the transcriptional changes of twelve selected DEGs induced by SLCCNV infection. Close examination revealed that the expression levels of all the DEGs of the pathway Photosynthesis were downregulated upon SLCCNV infection. Most DEGs in the pathway Plant-pathogen interaction were upregulated, including some positive regulators of plant defenses. Moreover, the majority of DEGs in the MAPK signaling pathway-plant were upregulated.

Conclusion: Our findings indicates that SLCCNV actively interact with its cucurbitaceous plant host by suppressing the conversion of light energy to chemical energy and inducing immune responses. Our study not only provides new insights into the interactions between begomoviruses and host plants, but also adds to our knowledge on virus-plant interactions in general.

Keywords: Cucurbita pepo; Bipartite begomovirus; Plant-virus interaction; Squash leaf curl China virus; Transcriptional reprograming.

Fig. 1

Symptoms induced by SLCCNV in zucchini plants. Zucchini plants were inoculated with pBINPLUS (empty vector) or SLCCNV DNA-A + DNA-B. Symptoms of SLCCNV infection in zucchini plants showed dwarf, downward leaf curl and mosaic in young leaves and mosaic in old leaves. Pictures were taken at four weeks post inoculation

Fig. 2

Volcano plot of DEG analysis between pBINPLUS and SLCCNV treatments. Each point in the plot corresponds to a specific gene. Blue points (right side) indicate significantly upregulated genes, yellow points (left side) represent significantly downregulated genes, and gray points (middle) signify genes with no significant differences. The closer a point is to the edges and the top of the plot, the more pronounced its expression difference

Fig. 3

Distribution of the top 20 enriched KEGG pathways. The Y-axis represented the name of the pathway, and the X-axis indicated the rich factor of the pathway. The q value was indicated by the color of the dots, and the number of genes in each pathway was indicated by the size of the dots

Fig. 4

qRT-PCR validation of the fold change (SLCCNV vs. pBINPLUS) of DEGs. (A-D) DEGs in the pathway Photosynthesis; (E-H) DEGs in the pathway Plant-pathogen interaction; (I-L) DEGs in the pathway MAPK signaling pathway-plant. The number of replicates was 4 for RNA-seq, 5–6 for qRT-PCR

Fig. 5

Regulation of the expression of DEGs in photosynthesis pathway. The photosynthetic cascade is shown, followed by the list of important components. For each component, blue frames indicate downregulation of gene expression upon SLCCNV infection. Yellow fill-ins of the box indicate previously-identified transcripts, while green fill-ins indicate newly-found transcripts

Fig. 6

Regulation of the expression of DEGs in plant-pathogen interaction pathway. The signaling cascade is shown with the important components involved. For each component, blue and red frames indicate downregulation and upregulation of gene expression, respectively. Yellow fill-ins of the box indicate previously-identified transcripts, while green fill-ins indicate newly-found transcripts

Fig. 7

Regulation of the expression of DEGs in MAPK signaling pathway-plant. The signaling cascade is shown with the important components involved. For each component, blue and red frames indicate downregulation and upregulation of gene expression, respectively. Yellow fill-ins of the box indicate previously-identified transcripts, while green fill-ins indicate newly-found transcripts