Complexity and Local Specificity of the Virome Associated with Tospovirus-Transmitting Thrips Species

Abstract

Frankliniella occidentalis (western flower thrips=WFT) and Thrips tabaci (onion thrips=OT) are insect species that greatly impact horticultural crops through direct damage and their efficient vectoring of tomato spotted wilt virus and iris yellow spot virus. In this study we collected thrips of these species from 12 field populations in various regions in Italy. We also included one field population of Neohydatothrips variabilis (soybean thrips=ST) from the U.S.A. Total RNAseq from high-throughput sequencing (HTS) was used to assemble the virome and then we assigned putative viral contigs to each thrips sample by qRT-PCR. Excluding plant and fungal viruses, we were able to identify 61 viral segments, corresponding to 41 viruses: 14 were assigned to WFT, 17 to OT, one from ST and 9 viruses could not be assigned to any species based on our stringent criteria. All these viruses are putative representative of new species (with only the exception of a sobemo-like virus that is 100% identical to a virus recently characterized in ST) and some belong to new higher-ranking taxa. These additions to the viral phylogeny suggest previously undescribed evolutionary niches. Most of the Baltimore’s classes of RNA viruses were present (positive- and minus- strand and dsRNA viruses), but only one DNA virus was identified in our collection. Repeated sampling in a subset of locations in 2019 and 2020 and further virus characterization in a subset of four thrips populations maintained in laboratory allowed us to provide evidence of a locally persistent thrips core virome that characterizes each population. IMPORTANCE Harnessing the insect microbiome can result in new approaches to contain their populations or the damage they cause vectoring viruses of medical, veterinary, or agricultural importance. Persistent insect viruses are a neglected component of their microbiota. Here for the first time, we characterize the virome associated with the two model systems for tospovirus-transmitting thrips species, of utmost importance for the direct and indirect damage they cause to a number of different crops. The thrips virome here characterized includes several novel viruses, that in some cases reveal previously undescribed clades. More importantly, some of the viruses we describe are part of a core virome that is specific and consistently present in distinct geographical locations monitored over the years, hinting at a possible mutualistic symbiotic relationship with their host.

Discovery and Community Dynamics of Novel ssRNA Mycoviruses in the Conifer Pathogen Heterobasidion parviporum

“…The 3,960 nt long sequence of RNA2 includes Sanger confirmed 5 UTR and CDS and one complete ORF encoding a predicted protein of 1,228 aa (predicted M r = 134.058 kDa). Based on BlastX, the insect narna-like virus 1 (Chiapello et al, 2021) hosted by thrips (insect pest Frankliniella occidentalis) showed highest similarity with RNA2 of HetNlV1 (Table 1). Phylogenetic analysis showed placement of HetNlV1 in a highly supported cluster including viruses from Plasmopara viticola lesions and thrips (Chiapello et al, 2020(Chiapello et al, , 2021; Figure 2B).…”

“…High-throughput sequencing (HTS) studies have recently revolutionized our understanding on the virosphere and revealed numerous novel virus clades that await classification by the International Committee on Taxonomy of Viruses (ICTV). Among these are many new fungal narna-like viruses ( Chiapello et al, 2020 , 2021 ; Sutela et al, 2020 ; Chiba et al, 2021 ; Jia et al, 2021 ) and the unclassified virus group tentatively named “ambiviruses” recently detected in asco- and basidiomycetous fungi ( Sutela et al, 2020 ; Forgia et al, 2021 ; Linnakoski et al, 2021 ). The accumulating sequence information has also led to the recognition of new host taxa for viruses, for example, plants as hosts for mitoviruses ( Nibert et al, 2018 ) and fungi as hosts of ourmia-like viruses (now classified in the viral family Botourmiaviridae in order Ourlivirales ), and the re-classification of many fungal viruses, for example, the division of family Narnaviridae into Mitoviridae and Narnaviridae .…”

Natural Resources Resistance to Tomato Spotted Wilt Virus (TSWV) in Tomato (Solanum lycopersicum)

“…During the fruit-ripening period, the fruit has red-yellow or red-white ring spots and bright yellow ring markings, particularly the The rapid spread of Frankliniella occidentalis (Western flower thrips) carrying the TSWV has seriously harmed tomato cultivation and production. The TSWV reduces yield in large areas and the marketable value of tomato or even causes the death of tomato plants [25,26]. Numerous tomato plants (such as those that carry the Sw-5 gene) resistant to the TSWV have been screened, and many excellent reviews on the different aspects of TSWV biology, thrips vector-mediated transmission, resistance strategies, and plants' innate immunity to the TSWV have been published [10,[27][28][29][30][31][32][33].…”

“…Susceptible plants were inoculated with TSWV isolates at the four-, five, and six-leaf stages and cultivated for symptom development. Then, systemically infected plants were fed to the first instar larvae (0-2 h old) of Frankliniella occidentalis for 2 days to carry the TSWV isolates [26]. The viruliferous larvae were cultivated into adults on healthy plants.…”

Deep mining of the Sequence Read Archive reveals bipartite coronavirus genomes and inter-family Spike glycoprotein recombination

“…Following the emerging trend in virology, recently described nidoviruses have been discovered by bioinformatics analysis of next or third generation sequencing data from meta-genomic andtranscriptomics studies of diverse specimens [6,7,[21][22][23][24][25][26][27][28][29][30][31][32][33][34]. These data sets are composed of overlapping sequence fragments of variable lengths (so-called reads) of various origins that can be assembled into contigs, some of which may represent full-length or partial viral genomes.…”