{"title":"Virus-Induced Gene Silencing Simultaneously Exploits ‘Attract and Kill’ Traits in Plants and Insects to Manage Huanglongbing","authors":"Nabil Killiny, Yasser Nehela, Subhas Hajeri, Siddarame Gowda, Lukasz L Stelinski","doi":"10.1093/hr/uhae311","DOIUrl":null,"url":null,"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.","PeriodicalId":13179,"journal":{"name":"Horticulture Research","volume":null,"pages":null},"PeriodicalIF":8.7000,"publicationDate":"2024-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Horticulture Research","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1093/hr/uhae311","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0
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.
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.