Abstract
Tomato leaf curl New Delhi virus (ToLCNDV) emerged in the Mediterranean Basin in 2012 as the first DNA bipartite begomovirus (Geminiviridae family), causing severe yield and economic losses in cucurbit crops. A major resistance locus was identified in the wild melon accession WM-7 (Cucumis melo kachri group), but the mechanisms involved in the resistant response remained unknown. In this work, we used RNA-sequencing to identify disease-associated genes that are differentially expressed in the course of ToLCNDV infection and could contribute to resistance. Transcriptomes of the resistant WM-7 genotype and the susceptible cultivar Piñonet Piel de Sapo (PS) (C. melo ibericus group) in ToLCNDV and mock inoculated plants were compared at four time points during infection (0, 3, 6, and 12 days post inoculation). Different gene expression patterns were observed over time in the resistant and susceptible genotypes in comparison to their respective controls. Differentially expressed genes (DEGs) in ToLCNDV-infected plants were classified using gene ontology (GO) terms, and genes of the categories transcription, DNA replication, and helicase activity were downregulated in WM-7 but upregulated in PS, suggesting that reduced activity of these functions reduces ToLCNDV replication and intercellular spread and thereby contributes to resistance. DEGs involved in the jasmonic acid signaling pathway, photosynthesis, RNA silencing, transmembrane, and sugar transporters entail adverse consequences for systemic infection in the resistant genotype, and lead to susceptibility in PS. The expression levels of selected candidate genes were validated by qRT-PCR to corroborate their differential expression upon ToLCNDV infection in resistant and susceptible melon. Furthermore, single nucleotide polymorphism (SNPs) with an effect on structural functionality of DEGs linked to the main QTLs for ToLCNDV resistance have been identified. The obtained results pinpoint cellular functions and candidate genes that are differentially expressed in a resistant and susceptible melon line in response to ToLCNDV, an information of great relevance for breeding ToLCNDV-resistant melon cultivars.
Highlights
Melon (Cucumis melo L.) is one of the major cucurbit crops cultivated worldwide and with large diversification
Viral accumulation was low in both WM-7 and Piel de Sapo (PS) at the early stage of 3 dpi, but significant differences were observed in the course of the disease (Figure 1B)
The number of downregulated genes in PS did not show this increasing pattern with a maximum at 6 dpi (245, 440, and 181 downregulated genes at 3, 6, and 12 dpi, respectively) a slight increase was found in WM-7 (146, 132, and 215 Differentially expressed genes (DEGs)). These results suggest that Tomato Leaf curl New Delhi virus (ToLCNDV) infection causes a lower impact on the transcriptomic reorganization in WM-7 than in PS, consistent with similar studies comparing the response to begomoviruses in resistant and susceptible accessions (Allie et al, 2014; Zaidi et al, 2020)
Summary
Melon (Cucumis melo L.) is one of the major cucurbit crops cultivated worldwide and with large diversification It is highly appreciated for its nutritional profile and its sweet and aromatic flavor, and its production generates large profits to farmers in developing and industrialized countries. Tomato Leaf curl New Delhi virus (ToLCNDV) is a species of bipartite begomovirus (family Geminiviridae) naturally transmitted by the whitefly Bemisia tabaci (Gennadius) in a persistent manner. This virus has posed a major threat to melon crops in many countries of the Indian subcontinent since the earliest 2000s, but recently, a new recombinant strain has appeared in the Mediterranean basin that has generated a devastating disease to mainly melon and zucchini squash (Cucurbita pepo) crops (Juárez et al, 2014). The Mediterranean ToLCNDV strain has been designated as ToLCNDV-ES (Moriones et al, 2017)
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