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. 2023 Nov 30;15(12):2370.
doi: 10.3390/v15122370.

Enhanced Susceptibility to Tomato Chlorosis Virus (ToCV) in Hsp90- and Sgt1-Silenced Plants: Insights from Gene Expression Dynamics

Irene Ontiveros  1   2 , Noé Fernández-Pozo  1 , Anna Esteve-Codina  3 , Juan José López-Moya  2 , Juan Antonio Díaz-Pendón  1
Affiliations

Enhanced Susceptibility to Tomato Chlorosis Virus (ToCV) in Hsp90- and Sgt1-Silenced Plants: Insights from Gene Expression Dynamics

Irene Ontiveros et al. Viruses. .

Abstract

The emerging whitefly-transmitted crinivirus tomato chlorosis virus (ToCV) causes substantial economic losses by inducing yellow leaf disorder in tomato crops. This study explores potential resistance mechanisms by examining early-stage molecular responses to ToCV. A time-course transcriptome analysis compared naïve, mock, and ToCV-infected plants at 2, 7, and 14 days post-infection (dpi). Gene expression changes were most notable at 2 and 14 dpi, likely corresponding to whitefly feeding and viral infection. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses revealed key genes and pathways associated with ToCV infection, including those related to plant immunity, flavonoid and steroid biosynthesis, photosynthesis, and hormone signaling. Additionally, virus-derived small interfering RNAs (vsRNAs) originating from ToCV predominantly came from RNA2 and were 22 nucleotides in length. Furthermore, two genes involved in plant immunity, Hsp90 (heat shock protein 90) and its co-chaperone Sgt1 (suppressor of the G2 allele of Skp1) were targeted through viral-induced gene silencing (VIGS), showing a potential contribution to basal resistance against viral infections since their reduction correlated with increased ToCV accumulation. This study provides insights into tomato plant responses to ToCV, with potential implications for developing effective disease control strategies.

Keywords: Bemisia tabaci; Hsp90; Sgt1; ToCV; basal resistance; tomato.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Exploratory analysis of transcriptomic data. (A) Principal component analysis (PCA) of all replicates from naïve (no whitefly and no virus), Mock (non-viruliferous whiteflies), and ToCV (ToCV-viruliferous whiteflies) samples at 2, 7, and 14 days post-infection (dpi). (B) Number of up-regulated and down-regulated differentially expressed genes (DEGs) at each time point after ToCV infection. Red and blue bars represent numbers of up-regulated and down-regulated genes, respectively. Total indicates the total number of both up-regulated and down-regulated DEGs. (C) Venn diagram displaying the number of shared and distinct DEGs across the three specified time points.
Figure 2
Figure 2
Gene ontology (GO) enrichment analysis of the differentially expressed genes (DEGs) in response to ToCV infection at 2, 7, and 14 days post inoculation (dpi). Enrichment of GO terms among the up-regulated (A) and down-regulated (B) DEGs. Each cell is colored based on the number of genes associated with the respective GO term.
Figure 3
Figure 3
KEGG enrichment analysis. Top KEGG pathways enriched with up-regulated (A) and down-regulated (B) differentially expressed genes (DEGs) triggered by ToCV infection at 2, 7, and 14 days post-inoculation (dpi).
Figure 4
Figure 4
Global analysis of virus-derived small RNAs (vsRNAs) in tomato plants infected with ToCV. (A) Percentage of vsRNAs in the 20–25 nt reads pool mapped to RNA1 and RNA2 of the ToCV genome. (B) Single-nucleotide resolution maps of vsRNAs from tomato plants challenged by ToCV. Positive- and negative-strand reads are shown in blue and red, respectively. Genome organization of each viral genomic RNA is shown.
Figure 5
Figure 5
Impact of silencing of tomato Hsp90 and Sgt1 genes through virus-induced gene silencing on the susceptibility to ToCV infection. (A) Phenotypes observed in ToCV-infected tomato plants at 14 days post-inoculation (dpi) that were agroinfiltrated 7 days earlier with tobacco rattle virus (TRV) vector alone (TRV2), with the TRV Sgt1- and Hsp90-silencing constructs (TRV-Sgt1 and TRV-Hsp90) and mock-inoculated (Mock). (B) Relative accumulation of ToCV RNA at 12 dpi analyzed by reverse transcription–quantitative polymerase chain reaction (RT-qPCR). The plants were agroinfiltrated 7 days earlier with TRV2, TRV-Sgt1, TRV-Hsp90, or Mock. Values were normalized using tomato elongation factor 1-α and Sand as reference genes, with Mock serving as the calibrator. Error bars represent standard errors of five biological replicates and an asterisk indicates a significant difference according to one-way ANOVA with p < 0.05.
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