Brown Planthopper Nudivirus DNA Integrated in Its Host Genome

Abstract

The brown planthopper (BPH), Nilaparvata lugens (Hemiptera:Delphacidae), is one of the most destructive insect pests of rice crops in Asia. Nudivirus-like sequences were identified during the whole-genome sequencing of BPH. PCR examination showed that the virus sequences were present in all of the 22 BPH populations collected from East, Southeast, and South Asia. Thirty-two of the 33 nudivirus core genes were identified, including 20 homologues of baculovirus core genes. In addition, several gene clusters that were arranged collinearly with those of other nudiviruses were found in the partial virus genome. In a phylogenetic tree constructed using the supermatrix method, the original virus was grouped with other nudiviruses and was closely related to polydnavirus. Taken together, these data indicated that the virus sequences belong to a new member of the family Nudiviridae. More specifically, the virus sequences were integrated into the chromosome of its insect host during coevolution. This study is the first report of a large double-stranded circular DNA virus genome in a sap-sucking hemipteran insect. IMPORTANCEThis is the first report of a large double-stranded DNA virus integrated genome in the planthopper, a plant sap-sucking hemipteran insect. It is an exciting addition to the evolutionary story of bracoviruses (polydnaviruses), nudiviruses, and baculoviruses. The results on the virus sequences integrated in the chromosomes of its insect host also represent a story of successful coevolution of an invertebrate virus and a plant sap-sucking insect. Brown planthoppers (BPH) (Nilaparvata lugens) are insect herbivores that feed mainly on rice. They damage rice plants by sucking sap from the vascular bundle and by transmitting the rice ragged stunt virus (RRSV) and rice grassy stunt virus (RGSV) (1). In addition, three commensal viruses have been characterized in BPH, i.e., Nilaparvata lugens reovirus (NLRV) (2), himetobi P virus (HiPV), and Nilaparvata lugens commensal X virus (NLCXV) (3). Recently, an iflavirus found in the honeydews of BPH was reported as Nilaparvata lugens honeydew virus 1 (NLHV-1) (4). These viruses infect BPH without visible symptoms, raising the question of how the insect host copes with various foreign microbes.In our study on the whole genome sequence of BPH, sequences that likely belonged to a previously unknown virus were identified (5). Homology analysis indicated that the sequences came from an uncharacterized virus that was related to the family Nudiviridae. Nudiviruses (Latin nudi ϭ naked) are a highly diverse group of invertebrate viruses that have rod-shaped nucleocapsids and large, double-stranded DNA (dsDNA) genomes. They were once described as "nonoccluded baculoviruses" but were later excluded from the family Baculoviridae (6). These baculovirus-like particles have been reported in a wide range of host species of insects and other arthropods (7, 8); however, although related to baculoviruses, they form a distinct lineage.To date, only a few nudiviruses have been well ...

The Genome of the Nucleopolyhedrosis-Causing Virus from Tipula oleracea Sheds New Light on the Nudiviridae Family

“…Based on the concatenated alignment of 37 nudivirus-related genes from 18 dsDNA viruses, including four endogenous nudiviruses (three bracoviruses and the endogenous nudivirus of N. lugens [NlENV]) (Table 5), a highly supported phylogenetic tree was obtained by maximum likelihood analyses. The interrelationships between baculovirus, nudivirus, bracovirus, and hytrosavirus families were in accordance with previous results (30,39,64). ToNV clearly belonged to the Nudiviridae clade and not to the Baculoviridae (Fig.…”

“…Surprisingly, two dipteran nudiviruses (ToNV and DiNV) clearly belong to different genera, which contrasts with the Alphanudivirus genus, which includes viruses infecting three insect orders. Nudiviruses also appear to be particularly prone to endogenization as recently shown with the sequences found in the planthopper genome, which derived from an Alphanudivirus (39). In an entirely independent event, the endogenization and domestication of a nudivirus more related to ToNV than to HzNVs or PmNV led to the evolution of bracoviruses (30,65).…”

“…The tree revealed that ToNV was distant from all other nudiviruses but more closely related to the HzNV-PmNV clade, to which bracoviruses were also related (30). The fruit fly virus DiNV was close to OrNV and belonged to the Alphanudivirus genus, from which NlENV originated (39). This indicated that two nudiviruses infecting the same host order (Diptera) could be distantly related.…”

“…These three viral families, which evolved over 310 million years ago (MYA) (30), share a number of structural and genomic features while retaining lineage specific characteristics (26,28). In particular, nudiviruses can durably integrate into the genome of their hosts, as has occurred in braconid wasps ϳ103 MYA, leading to bracovirus symbiosis (37,38), a phenomenon that has also occurred independently in the brown planthopper (39).…”

Transcription of densovirus endogenous sequences in the Myzus persicae genome

“…Deep-sequence analysis of insect genomes has revealed that they may contain integrated viral sequences that are not of retroviral origin (Katzourakis & Gifford, 2010;Liu et al, 2011b;Thézé et al, 2011). These ancestral endogenous sequences share similarity with viruses in different families: ssDNA viruses (family Parvoviridae), dsDNA viruses (families Baculoviridae, Polydnaviridae and Nudiviridae), reverse-transcribed DNA viruses (family Hepadnaviridae), ssRNA positive-sense (family Flaviviridae) or negative-sense (families Rhabdoviridae and Orthomyxoviridae) viruses, and dsRNA viruses (family Reoviridae) (Bézier et al, 2009;Cheng et al, 2014;Katzourakis & Gifford, 2010;Liu et al, 2011c;Thézé et al, 2011). Integration of such a great diversity of viral sequences suggests that many different replication strategies can induce integration of these sequences into host genomes.…”