Virus-Induced Gene Silencing Simultaneously Exploits ‘Attract and Kill’ Traits in Plants and Insects to Manage Huanglongbing

IF 8.7 1区 农林科学 Q1 Agricultural and Biological Sciences Horticulture Research Pub Date : 2024-11-07 DOI:10.1093/hr/uhae311
Nabil Killiny, Yasser Nehela, Subhas Hajeri, Siddarame Gowda, Lukasz L Stelinski
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Abstract

The vector-borne disease Huanglongbing (HLB) causes severe economic losses to citrus production worldwide with no available cure. Herein, we applied virus-induced gene silencing technology to engineer citrus that preferentially attracted and specifically killed Diaphorina citri, the vector associated with HLB. We engineered the infectious citrus tristeza virus (CTV-T36) clone to carry three truncated genes. The triple construct (CTV-tAwd-tWnt-tPDS) produces small interfering RNAs (siRNAs) against phytoene desaturase, PDS, to yield a phenotype with visual, olfactory, and gustatory cues that preferentially attracted D. citri. In addition, siRNAs targeted two genes related to flight in D. citri, abnormal wing disc (DcAwd) and wingless (DcWnt), that caused wing malformations and decreased survival in psyllids that fed on plants inoculated with the engineered virus. During two successive generations, D. citri reared on CTV-tAwd-tWnt-tPDS-inoculated plants exhibited higher mortality across life stages as well as reduced fecundity and fertility as compared with those reared on non-infected plants or CTV-wt-inoculated plants. Furthermore, CTV-tAwd-tWnt-tPDS-inoculated plants shortened the lifespan of D. citri by more than 20 days. Morphological abnormalities were noted in those adults that did successfully emerge on plants inoculated with CTV-tAwd-tWnt-tPDS, including cocked wings with a bowl-shaped depression and/or a convex shape. Phloem sap from CTV-tAwd-tWnt-tPDS-inoculated plants decreased the survival of D. citri adults, confirming that siRNAs were present in the sap of these plants. Collectively, we provide proof of concept for a novel variant of the attract-and-kill method where the cultivated crop is potentially transformed into a hyper-attractive population and transmission sink for a phytopathogen vector.
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病毒诱导的基因沉默同时利用植物和昆虫的 "引诱和杀灭 "特性管理黄龙病
病媒传播的黄龙病(HLB)给全世界的柑橘生产造成了严重的经济损失,而且目前尚无根治方法。在本文中,我们应用病毒诱导基因沉默技术来设计柑橘,使其优先吸引并特异性杀死与黄龙病相关的病媒--柑橘蝽。我们设计了传染性柑橘三联病毒(CTV-T36)克隆,使其携带三个截短基因。三重构建体(CTV-tAwd-tWnt-tPDS)可产生针对植物烯去饱和酶(PDS)的小干扰 RNA(siRNA),从而产生一种具有视觉、嗅觉和味觉线索的表型,优先吸引柑橘蝇。此外,siRNAs 还针对了两个与 D. citri 飞行有关的基因,即异常翅盘(DcAwd)和无翅(DcWnt),这两个基因会导致以接种了工程病毒的植物为食的稻飞虱翅膀畸形并降低存活率。在连续两代中,在接种了 CTV-tAwd-tWnt-tPDS 的植株上饲养的柠檬蚜与在未感染植株或接种了 CTV-wt 的植株上饲养的柠檬蚜相比,各生命阶段的死亡率都较高,繁殖力和生育力也有所下降。此外,接种 CTV-tAwd-tWnt-tPDS 的植株使柠檬蝇的寿命缩短了 20 多天。在接种了 CTV-tAwd-tWnt-tPDS 的植株上成功萌发的成虫出现了形态异常,包括带有碗状凹陷和/或凸形的鸡翅。接种了 CTV-tAwd-tWnt-tPDS 的植株的韧皮部汁液降低了柠檬蝇成虫的存活率,证实了 siRNA 存在于这些植株的汁液中。总之,我们为吸引-杀灭法的一种新变体提供了概念证明,在这种变体中,栽培作物有可能转变为植物病原体载体的超吸引种群和传播汇。
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来源期刊
Horticulture Research
Horticulture Research Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
11.20
自引率
6.90%
发文量
367
审稿时长
20 weeks
期刊介绍: Horticulture Research, an open access journal affiliated with Nanjing Agricultural University, has achieved the prestigious ranking of number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2022. As a leading publication in the field, the journal is dedicated to disseminating original research articles, comprehensive reviews, insightful perspectives, thought-provoking comments, and valuable correspondence articles and letters to the editor. Its scope encompasses all vital aspects of horticultural plants and disciplines, such as biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.
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