Chemosensory protein regulates the behavioural response of Frankliniella intonsa and Frankliniella occidentalis to tomato zonate spot virus-Infected pepper (Capsicum annuum)

文献类型： 外文期刊

第一作者： Li, Heng

作者： Li, Heng;Chen, Yixin;Lu, Chengcong;Linghu, Tingting;Wei, Hui;Fan, Xiaojing;Chen, Yong;Tian, Houjun;Lin, Shuo;Wang, Liang;Wei, Hui;Chen, Yong;Linghu, Tingting;Fan, Xiaojing;Zheng, Xue

作者机构：

期刊名称：PLOS PATHOGENS （ 影响因子：6.7； 五年影响因子：6.7 ）

ISSN： 1553-7366

年卷期： 2023 年 19 卷 5 期

页码：

收录情况： SCI

摘要： Author summaryArboviruses rely on insect vectors for their transmission, and promote disease transmission by influencing insect behaviour after infecting plant hosts. However, the detailed olfactory responses involved in this process are poorly understood. Here, we demonstrate that a persistent plant virus induces the production of a unique volatile in its host plant that is recognized by a key olfactory protein in its insect vector. Furthermore, this unique volatile induced by virus infection fits deep inside the binding pocket of its cognate olfactory protein, where it interacts with several hydrophilic residues. This work reveals that a plant virus can manipulate the behaviour of its insect vectors, suggesting the modification of insect behaviour by chemicals as a management program to control the spread of plant viruses. Many herbivorous insects rely on plant volatiles to locate their host plants. Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatile cis-3-hexenal, which is recognized by chemosensory protein 1 of the thrips Frankliniella intonsa (FintCSP1), are more attractive to F. intonsa than the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna of F. intonsa. Silencing of FintCSP1 significantly decreased electroantennogram responses of F. intonsa antennae to cis-3-hexenal and impaired thrips' responses to TZSV-infected pepper plants and cis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven alpha-helixes and two disulfide bridges. Molecular docking analysis suggested that cis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical for cis-3-hexenal binding. Furthermore, CSP of F. occidentalis (FoccCSP) is also a key olfactory protein involved in modulating the behaviour of F. occidentalis to TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs to cis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission.

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