Identification of novel resistance sources and insights into resistance against cucumber green mottle mosaic virus in watermelon germplasms

doi:10.1016/j.jia.2026.09.009

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Identification of novel resistance sources and insights into resistance against cucumber green mottle mosaic virus in watermelon germplasms

Zhiling Liang^1,2, Liming Liu¹, Luyi Zhao¹, Leiyan Yan³, Yanfei Geng¹, Yaoxing Zang¹, Yuhong Wang³, Qinsheng Gu^1,4^#, Baoshan Kang^1,2^#

¹Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Henan Key Laboratory of Fruit and Cucurbit Biology, Zhengzhou Henan, China

²Zhongyuan Research Center, Chinese Academy of Agricultural Sciences, Xinxiang, Henan, China

³Ningbo Key Laboratory of Characteristic Horticultural Crops in Quality Adjustment and Resistance Breeding, Ningbo Academy of Agricultural Sciences, Ningbo Zhejiang, China

⁴Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences, Xinjiang, China

Highlights

— Nine watermelon accessions exhibited segregation in response to CGMMV infection, comprising resistant, tolerant, or susceptible individuals.

— ZGCL22-P3 exhibited high resistance with no symptoms and near-undetectable CGMMV accumulation at 20 and 45 dpi.

— Resistant plants of ZGCL13-P3 exhibited minimal transcriptional changes, whereas tolerant plants of ZGCL13-P3 mainly activated phenylpropanoid- and lignin-associated pathways and susceptible plants of ‘Hongyihao’ mainly induced general stress responses.

Abstract
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摘要

黄瓜绿斑驳花叶病毒（CGMMV）属于烟草花叶病毒属（Tobamovirus），由于抗性资源有限，对全球西瓜生产构成严重威胁。本研究以来源于4个西瓜亚种（Citrullus lanatus、Citrullus amarus、Citrullus colocynthis、Citrullus mucosospermus）的40份西瓜种质材料为研究对象，通过接种CGMMV，结合植株发病表型观察与病毒积累量检测，并与感病对照材料比对，系统开展种质抗性鉴定评价。抗性鉴定结果表明，ZGCL22-P3在接种后20 d和45 d均无发病症状，病毒积累量极低，表现出高抗。此外，有9份材料在接种病毒后出现抗（耐）病与感病表型分离。在ZGCL13-P3和PI 388770的部分无症状植株中，病毒累积量在接种后20天和45天两个时间点均未检测到，表明这些材料可能携带抗病基因。其余30份材料对CGMMV均表现为感病。基于表型及病毒积累量差异，选择具有代表性的抗/耐病ZGCL13-P3植株和感病品种进行转录组分析，对比解析不同抗性表型西瓜植株的分子响应差异。RNA-seq结果显示，不同材料的防御策略存在显著差异。具体而言，CGMMV耐病的ZGCL13表现出大规模的转录重编程，苯丙烷途径相关酶活性增强，尤其是参与细胞壁木质化加固的PAL和LAC/PRX，表现为轻微症状且病毒积累较低；而感病品种则主要激活一般胁迫及激素信号途径，而非结构性防御。这些结果为西瓜抗CGMMV育种提供了宝贵的遗传资源，并揭示了潜在的育种靶点。

Abstract

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.

Keywords: CGMMV watermelon resistance germplasm tolerant transcriptome phenylpropanoid pathway Lignin

Online: 03 September 2026

Fund:

This work was funded by the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2022-ZFRI-09), Henan Province Science and Technology Research Project (252102110208), the Natural Science Foundation of China (U21A20229), the Ningbo Scientific and Technological Project (Grant No.2021Z006), and the Preparation and Application of Reference Materials for Quarantine Plant Viruses (2024HK174).

About author: Zhiling Liang, E-mail: liangzhiling666@163.com; #Correspondence Qinsheng Gu, E-mail: guqinsheng@caas.cn; Baoshan Kang, Tel: 13849001280, E-mail: kangbaoshan@caas.cn

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Zhiling Liang, Liming Liu, Luyi Zhao, Leiyan Yan, Yanfei Geng, Yaoxing Zang, Yuhong Wang, Qinsheng Gu, Baoshan Kang. 2026.

Identification of novel resistance sources and insights into resistance against cucumber green mottle mosaic virus in watermelon germplasms . Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.09.009

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