Cucumber green mottle mosaic virus (CGMMV) from the Tobamovirus genus poses a significant threat to global watermelon (Citrullus lanatus) production due to limited resistant resources. To identify CGMMV-resistant sources, 40 watermelon accessions, representing four subspecies: Citrullus lanatus, Citrullus amarus, Citrullus colocynthis, and Citrullus mucosospermus, were evaluated for resistance. The plants were inoculated with CGMMV and resistance was evaluated based on virus accumulation and visual symptoms compared with susceptible controls. ZGCL22-P3 showed no symptoms and had undetectable virus levels at 20- and 45-days post-inoculation (dpi), indicating high resistance. Nine accessions, including ZGCL13-P3, PI 388770, PI 386015, PI 220778, PI 195927, PI 537300, PI 386026, PI 386014, and PI 432337, exhibiting segregation in disease rating, resistant, tolerant, or susceptible individuals were observed, and ZGCL13-P3 displayed the lowest disease index among them. The viral accumulation in some asymptomatic ZGCL13-P3 and PI 388770 plants was undetectable at both 20 and 45 dpi, indicating high resistance to CGMMV. The remaining 30 accessions were susceptible to CGMMV. As tolerant individuals were present in all nine accessions, representative resistant and tolerant plants of ZGCL13-P3, along with the susceptible control ‘Hongyihao’, were specifically selected for transcriptome analysis, enabling a direct comparison of molecular responses among accessions. The CGMMV-tolerant ZGCL13-P3 exhibited large-scale transcriptional reprogramming, with enhanced phenylpropanoid enzyme activity, particularly PAL and LAC/PRX involved in reinforcing lignified cell walls, resulting in milder symptoms and lower virus accumulation, whereas susceptible variety was activated by general stress and hormone pathways instead of structural defenses. These findings highlight valuable genetic resources for breeding and provide novel targets for breeding virus‐resistant watermelon cultivars.
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