HMG-like DSP1 is a damage signal to mediate the western flower thrips, Frankliniella occidentalis, immune responses to tomato spotted wilt virus infection

Authors: CHUL-YOUNG, KIM - Andong National University; ABMED, SHABBIR - Andong National University; Stanley, David; KIM, YONGGYUN - Andong National University

Submitted to: Developmental and Comparative Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/2/2023
Publication Date: 4/3/2023
Citation: Chul-Young, K., Abmed, S., Stanley, D.W., Kim, Y. 2023. HMG-like DSP1 is a damage signal to mediate the western flower thrips, Frankliniella occidentalis, immune responses to tomato spotted wilt virus infection. Developmental and Comparative Immunology. 144. Article 104706. https://doi.org/10.1016/j.dci.2023.104706.
DOI: https://doi.org/10.1016/j.dci.2023.104706

Interpretive Summary: There are many kinds of plant killing viruses that lead to tremendous world-wide crop losses. Examples of the top 10 most important viruses include the cucumber mosaic virus, the potato virus X and the tomato spotted wilt virus. The tomato spotted wilt virus is a serious, global disease that destroys high-value crops, such as tomato and red pepper. The virus is transmitted among plants by small, feathery winged insects called thrips. Because thrips are highly effective carriers of the virus, there are real needs to understand how thrips acquire the virus, how the virus develops within thrips and how it is transmitted to healthy crop plants. Here, we report that juvenile thrips acquire the virus by feeding on virus-infected plants. Within the thrips, the virus multiplies many times in the juvenile insect intestine. As the thrips approach adulthood, the virus migrates within the body to the salivary glands. As the adults feed on the plants, the virus is transmitted with saliva to healthy plants, which leads to plant death. In this paper we identify a specific protein in the thrips that signals insect immune responses to the virus infection. At present, the thrip immune response is not sufficient to block transmission of the virus. The new knowledge of this protein will help scientists elongate thrip immune responses to the virus. The enhanced immune response will reduce the spread of the virus to healthy plants and reduce crop losses. This work will contribute to the global effort to increase availability of healthy, high-quality foods using environmentally sustainable practices. Such improvements in plant health are necessary for enhanced agricultural production to support a growing human population.

Technical Abstract: Tomato spotted wilt virus (TSWV) causes a serious plant disease and is transmitted by specific thrips including the western flower thrips, Frankliniella occidentalis. The persistent and circulative virus transmission leads to immune defenses within hosts. We investigated the immune responses to TSWV infection in F. occidentalis. Immunofluorescence assay demonstrated viral infection in thrips larval dguts, which is propagated to the salivary gland in adults. In the larval midgut, TSWV infection led to the release of DSP1, a damage associated molecular pattern from the gut epithelium into the hemolymph. DSP1 up-regulated PLA2 activity, which leads to biosynthesis of eicosanoids that activate cellular and humoral immune responses. Phenoloxidase (PO) activity was enhanced following induction of PO and its activating protease gene expression. Antimicrobial peptide genes and dual oxidase, which produces reactive oxygen species, were induced by infecction. Expression of four caspase genes increased and TUNEL assay onfirmed apoptosis in the larval midgut after the virus infection. These immune responses to viral infection were significantly suppressed by the inhibition of DSP1 release. We infer that TSWV infection induces F. occidentalis immune responses, which are activated by the release of DSP1 from infection foci within midguts.