Simultaneous silencing of ten essential Sclerotinia sclerotiorum genes via spray- and host-induced gene silencing enhances against Sclerotinia stem rot resistance in oilseed rape

doi:10.1016/j.jia.2026.02.007

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Simultaneous silencing of ten essential Sclerotinia sclerotiorum genes via spray- and host-induced gene silencing enhances against Sclerotinia stem rot resistance in oilseed rape

Sichao Ren¹^*, Ying Zhang²^*, Yi Ye¹, Wenjing Huang¹, Wenxin Liu¹, Shengliang Yin¹, Yang Yang¹, Yu Liu¹, Jialin Fan¹, Yumei Wang¹, Youping Wang^1,3, Li Lin¹^#, Jian Wu¹^#

¹Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China

²Institute of Agricultural Sciences for Lixiahe Region in Jiangsu, Yangzhou 225007, China

³Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, Yangzhou University, Yangzhou 225009, China

Highlights

A 1,250-bp chimeric dsRNA simultaneously targeting ten Sclerotinia sclerotiorum genes effectively suppresses fungal development and pathogenicity.

Both spray-induced (SIGS) and host-induced (HIGS) gene silencing confer enhanced resistance to Sclerotinia stem rot in oilseed rape.

HIGS transgenic lines show stable, heritable resistance across multiple generations without compromising yield performance.

Abstract
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摘要

由坏死营养型真菌核盘菌（Sclerotinia sclerotiorum）引起的菌核病（Sclerotinia stem rot），是油菜（Brassica napus）在生产中最具危害性的病害之一。现有的油菜品种及其近缘种中缺乏有效抗源，迄今尚未发现能够赋予完全抗性的基因。为提高油菜对菌核病的抗性，本研究采用多靶标RNA干扰（RNAi）策略，设计并构建了一段可同时靶向核盘菌10个关键基因的嵌合双链RNA（dsRNA），其中包括8个与核盘菌生长发育相关的基因（SsChsI–VII、SsGas1）和2个与核盘菌致病性相关的基因（SsPG1、SsOAH1）。随后，分别通过喷施诱导基因沉默（spray-induced gene silencing, SIGS）和宿主诱导基因沉默（host-induced gene silencing, HIGS）两种技术对其防控效果进行分析。该嵌合dsRNA全长1,250 bp，由10个分别对应不同靶基因的125 bp片段串联组成。体外实验结果显示，该嵌合dsRNA处理可使核盘菌中9个靶基因的表达量下调50%以上，说明核盘菌能够有效摄取并加工长链dsRNA。经SIGS处理后，烟草和油菜植株的病斑面积及真菌生物量均显著降低。HIGS转基因油菜能够稳定产生针对靶基因的特异性小干扰RNA（siRNA），显著抑制核盘菌靶基因的表达，进而降低草酸积累和聚半乳糖醛酸酶活性，并抑制菌丝生长。HIGS转基因油菜对菌核病的抗性显著提高，且抗性在T₂至T₅代稳定遗传。在T₅代中，叶片病斑面积和茎秆病斑长度分别较对照减少38.9%–59.1%和43.2%–65.8%。综上，HIGS在不影响产量和品质的情况下赋予植株稳定且可遗传的抗病性，而SIGS则提供了一种快速、非转基因的防控途径。本研究验证了长链嵌合dsRNA在多基因同时沉默中的有效性，为提升油菜对菌核病的抗性提供了新的防控策略。

Abstract

Sclerotinia stem rot (SSR) is caused by the necrotrophic fungus Sclerotinia sclerotiorum and threatens global oilseed rape (Brassica napus) production. Moreover, researchers have not yet identified a gene that confers complete resistance. Here, we developed a multi-target RNA interference (RNAi) strategy to enhance plant resistance by simultaneously silencing eight fungal genes involved in development (SsChsI–VII, SsGas1) and two involved in pathogenicity (SsPG1, SsOAH1) of S. sclerotiorum. Accordingly, we designed a 1,250-bp chimeric double-stranded RNA (dsRNA) consisting of ten 125-bp fragments each targeting a different gene, and evaluated its effectiveness using spray-induced gene silencing (SIGS) and host-induced gene silencing (HIGS) via stable transformation. In vitro application of the chimeric dsRNA resulted in >50% downregulation of nine target genes, indicating efficient uptake and processing by S. sclerotiorum. Both lesion area and fungal biomass were significantly lower in Nicotiana benthamiana and oilseed rape plants following SIGS. Moreover, stable transgenic plants for HIGS effectively generated gene-specific short interfering RNAs and exhibited an increase in resistance from the T₂ to T₅ generations, with lesions that were 38.9–59.1% smaller in leaves and 43.2–65.8% smaller in stems in the T₅ generation compared with the control plants. Gene silencing resulted in lower oxalic acid accumulation, decreased polygalacturonase activity, and impaired hyphal development, suggesting interference with multiple fungal infection pathways. Notably, HIGS conferred stable, heritable resistance without yield penalty, whereas SIGS provided rapid, nontransgenic protection. This study demonstrates the effectiveness of long chimeric dsRNAs for multi-target gene silencing and highlights a promising RNAi-based strategy for improving disease resistance in oilseed rape, possibly in combination with natural quantitative resistance loci.

Keywords: Sclerotinia sclerotiorum Brassica napus host-induced gene silencing spray-induced gene silencing chimeric dsRNA multi-target gene silencing

Online: 05 February 2026

Fund:

This study was supported by the National Natural Science Foundation of China (32072020 and 32272112 to J.W.), the Natural Science Foundation of Jiangsu Province, China (BK20240046 to J.W., BE2022340 to Y.W.), the Graduate Research & Practice Innovation Program of Jiangsu Province, China (Yangzhou University, SJCX21_1599 to S.R.), and the Priority Academic Program Development of Jiangsu Higher Education Institutions, China.

About author: #Correspondence Jian Wu, Tel: +86-514-87979343, E-mail: wu_jian@yzu.edu.cn; Li Lin, Tel: +86-514-87997303, E-mail: ll@yzu.edu.cn *These authors contributed equally to this work.

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Sichao Ren, Ying Zhang, Yi Ye, Wenjing Huang, Wenxin Liu, Shengliang Yin, Yang Yang, Yu Liu, Jialin Fan, Yumei Wang, Youping Wang, Li Lin, Jian Wu. 2026. Simultaneous silencing of ten essential Sclerotinia sclerotiorum genes via spray- and host-induced gene silencing enhances against Sclerotinia stem rot resistance in oilseed rape. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.02.007

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