Engineering an efficient tomato spotted wilt virus mini-replicon system for high-throughput antiviral compound discovery

doi:10.1016/j.jia.2026.02.025

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Engineering an efficient tomato spotted wilt virus mini-replicon system for high-throughput antiviral compound discovery

Xingwang Zhang^1,²^*, Nan Zhou^1,²^*, Yulong Yuan^1,², Qinhai Liu^1,², Tianyi Zhang^1,², Shenghan Zang^1,², Yangliu Dai^1,², Baoyue Zhang^1,², Jia Li^1,², Min Zhu^1,², Xiaorong Tao^1,², Mingfeng Feng^1,²^#

¹State Key Laboratory of Agricultural and Forestry Biosecurity, Nanjing Agricultural University, Nanjing 210095, China

²Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China

Highlights

First establishment of a plant negative-strand RNA virus reverse genetics system in the absence of viral suppressors of RNA silencing (VSRs).

Development of a dual-vector-driven mini-replicon system enabling high-throughput screening of antiviral agents for sustainable crop protection.

Abstract
References

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摘要

番茄斑萎病毒（tomato spotted wilt virus, TSWV）是危害最严重的植物负义RNA病毒之一，能够侵染超过80个科的1000多种植物，并经由蓟马以持久增殖型方式传播。该病毒侵染可导致多种蔬菜和花卉作物严重发病并造成显著产量损失，对全球粮食安全构成持续威胁，因此亟需建立高效的抗病毒药剂筛选平台，对保障作物健康和粮食安全具有重要意义。携带报告基因的病毒反向遗传学体系可为抗病毒药剂筛选提供高效、简便、高通量的技术体系。目前，已有的TSWV反向遗传学体系需要将病毒编码的核衣壳蛋白（N）、RNA依赖的RNA聚合酶（RdRp或L）、病毒全长基因组RNA以及病毒沉默抑制子等多组分在同一植物细胞中共递送和共表达，操作繁琐且病毒侵染效率较低。本研究通过系列方法优化，在无病毒RNA沉默抑制子的条件下共表达TSWV的SR_(+)eGFP复制子与L_(+)opt基因组，成功构建了一种简化的TSWV微型复制子反向遗传学体系。基于该体系，本研究首先明确了运动蛋白NSm与M_(-)opt基因组均能显著增强TSWV微型复制子的复制效率及其细胞间运动能力，进一步构建了串联表达载体SR_(+)eGFP-M_(-)opt，最终创建了一套双载体驱动的TSWV反向遗传学新体系。值得注意的是，该系统在不依赖任何RNA沉默抑制子的情况下，实现了病毒100%的系统性侵染效率，这在植物负链RNA病毒的反向遗传学研究中尚属首次。基于TSWV微型复制子报告体系，建立了农杆菌浸润介导的半叶法抗病毒剂筛选技术平台。鉴定出6种具有潜在抗TSWV活性的药剂，包括利巴韦林、宁南霉素、壳寡糖、纤维二糖、印楝素和硫酸铜。选择利巴韦林作为抗病毒候选药剂，并进一步评估了该药剂对TSWV微型复制子浸润和毒源机械摩擦接种植物均具有显著地抗病毒作用。本研究建立的TSWV微型复制子系体系可用于大规模筛选抗病毒药剂，可在2天内通过SR_(+)eGFP-M_(-)opt报告载体的eGFP荧光来判断候选药剂的抗病毒效果。本研究不仅为植物负链RNA病毒的基因功能研究提供了一套新的反向遗传学操作工具，也为高通量筛选抗病毒药剂提供了高效、实用的技术平台。

Abstract

Plant viral diseases pose a persistent threat to global agriculture, requiring efficient platforms for antiviral agent screening to ensure sustainable crop protection. Here, we developed a simplified mini-replicon reverse genetics (RG) system for tomato spotted wilt virus (TSWV) based on co-expression of SR_(+)eGFP replicon and L_(+)opt genome in the absence of viral suppressors of RNA silencing (VSRs). Using this system, we demonstrated that the movement protein NSm and M_(-)opt genome significantly enhance both the replication and cell-to-cell movement of the TSWV mini-replicon. We further constructed a tandem expression vector (SR_(+)eGFP-M_(-)opt), and established a novel dual-vector-driven TSWV RG system. Notably, this system achieved 100% systemic infection efficiency without requiring any VSR. This is unprecedented for plant negative-strand RNA virus reverse genetics. This optimized system enabled the screening of antiviral agents, among which ribavirin, ningnanmycin, chitooligosaccharide, cellobiose, azadirachtin, and copper sulfate (CuSO₄) potently inhibited TSWV infection. Our study provides a new RG manipulation tool for functional genomics of plant negative-strand RNA viruses (NSVs) and a powerful platform for high-throughput antiviral agents discovery.

Keywords: plant negative-stranded RNA viruses reverse genetics system tomato spotted wilt virus antiviral agents

Online: 10 February 2026

Fund:

This work was supported by grants from the National Natural Science Foundation of China (32430088, 32470165, and 32220103008), the National Key Research and Development Program of China (2023YFD1401000), the Fundamental and Interdisciplinary Disciplines Breakthrough Plan of the Ministry of Education of China (JYB2025XDXM703), the Joint Research Program of State Key Laboratory of Agricultural and Forestry Biosecurity (SKLJRP2506), the Fundamental Research Funds for the Central Universities (KJYQ2025048), Yunnan Seed Laboratory (Grant No. 202205AR070001), the key projects of YNTC (2025530000241001).

About author: #Correspondence Mingfeng Feng: E-mail: fengmingfeng@njau.edu.cn * These authors contributed equally to this paper.

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Xingwang Zhang, Nan Zhou, Yulong Yuan, Qinhai Liu, Tianyi Zhang, Shenghan Zang, Yangliu Dai, Baoyue Zhang, Jia Li, Min Zhu, Xiaorong Tao, Mingfeng Feng. 2026. Engineering an efficient tomato spotted wilt virus mini-replicon system for high-throughput antiviral compound discovery. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.02.025

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