Thrips as the Transmission Bottleneck for Mixed Infection of Two Orthotospoviruses

Abstract

Mixed infections provide opportunities for viruses to increase genetic diversity by facilitating genomic reassortment or recombination, and they may lead to the emergence of new virus species. Mixed infections of two economically important orthotospoviruses, Tomato spotted wilt orthotospovirus (TSWV) and Impatiens necrotic spot orthotospovirus (INSV), were found in recent years, but no natural reassortants between INSV and TSWV were ever reported. The goal of this study was to establish how vector preferences and the ability to transmit INSV and TSWV influence transmission and establishment of mixed infections. Our results demonstrate that thrips prefer to oviposit on TSWV and INSV mixed-infected plants over singly infected or healthy plants, providing young nymphs with the opportunity to acquire both viruses. Conversely, we observed that thrips served as a bottleneck during transmission and favored transmission of one of the two viruses over the second one, or over transmission of both viruses simultaneously. This constraint was relaxed in plants, when transmission of TSWV and INSV occurred sequentially, demonstrating that plants serve as orthotospovirus permissive hosts, while thrips serve as a bottleneck. Viral fitness, as measured by virus replication, transmission, and competition with other viral strains, is not well studied in mixed infection. Our study looks at the success of transmission during mixed infection of orthotopoviruses, enhancing the understanding of orthotospovirus epidemiology and evolution.

The Infection Route of Tomato Zonate Spot Virus in the Digestive System of Its Insect Vector Frankliniella occidentalis

“…Thrips are the primary vectors for Orthotospoviruses , and they also serve as important hosts that provide sites for viral replication ( Rotenberg et al, 2015 ; Gupta et al, 2018 ; Rotenberg and Whitfield, 2018 ). Understanding the interactions between thrips and Orthotospoviruses is a key to controlling the diseases caused by these viruses, which have been the focus of much research ( Zhao and Rosa, 2020 ; Chen et al, 2021 ; Mou et al, 2021 ).…”

Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

“…Co-infections of plant viruses can be propagated by vectors that acquired virions from co-infected plants, sequentially from singly infected plants, or by multiple vector individuals that acquired different viruses. Vector acquisition of two viruses does not ensure both will be transmitted, and the presence of two viruses can alter transmission rates of one or both viruses 4,10,11,22–32,34–41,48–51 . Once acquired, two viruses may compete for binding sites required for retention in and transmission from their vectors 6,29,33,37,49,52 .…”

“…Co-infections of plant viruses can be propagated by vectors that acquired virions from co-infected plants, sequentially from singly infected plants, or by multiple vector individuals that acquired different viruses. Vector acquisition of two viruses does not ensure both will be transmitted, and the presence of two viruses can alter transmission rates of one or both viruses 4,10,11,[22][23][24][25][26][27][28][29][30][31][32][34][35][36][37][38][39][40][41][48][49][50][51] .…”

“…A majority of studies on mixed infections examine within plant-host dynamics of two viruses and their outcomes on disease severity and viral fitness [2][3][4][5][6][7][8] . Comparatively few studies use insect vector-transmission or examine vector-related effects 10,11,[22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41] . This study was conducted to examine how the manner of acquisition and inoculation of two viruses by their common vector affects propagation of co-infections in their plant hosts.…”

Analysis of the Defence Responses to Tomato Spotted Wilt Orthotospovirus (TSWV) and Hippeastrum Chlorotic Ringspot Orthotospovirus (HCRV) Infection in Capsicum Annuum Based on Transcriptome

“…According to factors such as the degree of damage and host range, 68 kinds of viruses in the world infect peppers [1]. Tomato spotted wilt orthotospovirus (TSWV) and Hippeastrum chlorotic ringspot orthotospovirus (HCRV) are orthotospoviruses that are transmitted by thrips (Thysanoptera) and are able to infect over 900 kinds of plant species within more than 90 families [2,3]. TSWV, Impatiens necrotic spot orthotospovirus (INSV) [4], Groundnut ringspot orthotospovirus (GRSV) [5], Watermelon silver mottle orthotospovirus (WSMoV), Tomato chlorotic spot orthotospovirus (TCSV) [6], Groundnut bud necrosis orthotospovirus (GBNV) [5], Pepper necrotic spot orthotospovirus (PNSV), Pepper chlorotic spot orthotospovirus (PCSV), Capsicum chlorosis orthotospovirus (CaCV) [7], Alstroemeria necrotic streak orthotospovirus (ANSV) [8], and Chilli yellow ringspot orthotospovirus (CYRSV) [9] can infect peppers, causing pepper leaf chlorosis, necrosis, concentric rings, necrotic spots, and pepper fruit deformity, which seriously affect yield and quality [10].…”