Abstract

DNA methylation is an important epigenetic mark associated with plant immunity, but little is known about its roles in viral infection of watermelon. We carried out whole-genome bisulfite sequencing of watermelon leaves at 0 h (ck), 48 h, and 25 days post-inoculation with Cucumber green mottle mosaic virus (CGMMV). The number of differentially methylated regions (DMRs) increased during CGMMV infection and 2788 DMR-associated genes (DMGs) were screened out among three libraries. Most DMRs and DMGs were obtained under the CHH context. These DMGs were significantly enriched in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways of secondary biosynthesis and metabolism, plant–pathogen interactions, Toll-like receptor signaling, and ABC transporters. Additionally, DMGs encoding PR1a, CaMs, calcium-binding protein, RIN4, BAK1, WRKYs, RBOHs, STKs, and RLPs/RLKs were involved in the watermelon–CGMMV interaction and signaling. The association between DNA methylation and gene expression was analyzed by RNA-seq and no clear relationship was detected. Moreover, downregulation of genes in the RdDM pathway suggested the reduced RdDM-directed CHH methylation plays an important role in antiviral defense in watermelon. Our findings provide genome-wide DNA methylation profiles of watermelon and will aid in revealing the molecular mechanism in response to CGMMV infection at the methylation level.

Highlights

  • Cucumber green mottle mosaic virus (CGMMV) is a member of the Tobamovirus genus that produces typical mosaic patterning on infected plants

  • In CGMMV-infected watermelon, mottling and mosaicism develop on the leaves of young plants, brown necrotic lesions occur in the stems and peduncles, and sponginess, rotting, and dirty-red discolorations are seen in the flesh [6]

  • We found that DMR-associated genes (DMGs) encoding CaM-like protein, calcium-binding protein, WRKYs, PR1a, respiratory burst oxidase homolog protein (RBOH), cyclic nucleotide-gated ion channel protein (CNGC), RIN4, and BRASSINOSTEROID INSENSITIVE 1-associated receptor kinase 1 (BAK1) were involved in plant–pathogen interaction pathways, and most of these genes were hypermethylated for 25d_ck and hypomethylated for 25d_48h (Table S4)

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Summary

Introduction

Cucumber green mottle mosaic virus (CGMMV) is a member of the Tobamovirus genus that produces typical mosaic patterning on infected plants. It was first reported in England in 1935 [1]. The diversity of CGMMV strains, including CV3, CV4, watermelon strain, Yodo strain, Indian C strain, and muskmelon strain have been found to cause serious diseases in cucurbits, diminishing their fruit yields and quality [1,2,3,4,5]. In CGMMV-infected watermelon, mottling and mosaicism develop on the leaves of young plants, brown necrotic lesions occur in the stems and peduncles, and sponginess, rotting, and dirty-red discolorations are seen in the flesh [6]. CGMMV management primarily relies on measures of cultural, biological, and host resistance [6]

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