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J Virol. 2019 Jan 9. pii: JVI.01516-18. doi: 10.1128/JVI.01516-18. [Epub ahead of print]

Horizontal transfer of a retrotransposon from the rice planthopper to the genome of an insect DNA virus.

Yang Q1,2,3, Zhang Y2,3, Andika IB4, Liao Z3,5, Kondo H4, Lu Y2,3, Cheng Y2,3, Li L6, He Y3, He Y2,3, Qi Y2,3, Sun Z2,3, Wu Y1, Yan F2,3, Chen J7,2,3, Li J8,3.

Author information

1
Plant Protection College, Shenyang Agricultural University, Shenyang 110866, China.
2
Institute of Plant Virology, Ningbo University, Ningbo 315211, China.
3
The State Key Laboratory Breeding Base for Sustainable Control of Pest and Disease, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China.
4
Institute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan.
5
Central Laboratory of Zhejiang Academy of Agricultural Sciences, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China.
6
College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China.
7
Plant Protection College, Shenyang Agricultural University, Shenyang 110866, China jpchen2001@126.com lijunmin@nbu.edu.cn.
8
Institute of Plant Virology, Ningbo University, Ningbo 315211, China jpchen2001@126.com lijunmin@nbu.edu.cn.

Abstract

Horizontal transfer of genetic materials between virus and host have been frequently identified. Three rice planthoppers, Laodelphax striatellus, Nilaparvata lugens, and Sogatella furcifera are agriculturally important insects because they are destructive rice pests and also the vector of a number of phytopathogenic viruses. In this study, we discovered that a small region (∼300 nt) of the genome of invertebrate iridescent virus 6 (IIV-6, genus Iridovirus, family Iridoviridae), a giant DNA virus that infects invertebrates but is not known to infect planthoppers, is highly homologous to the sequences present in high copy numbers in these three planthopper genomes. These sequences are related to the short interspersed nuclear elements (SINEs), a class of non-LTR retrotransposon (retroposon), suggesting a horizontal transfer event of a transposable element from the rice planthopper genome to IIV-6 genome. In addition, a number planthopper transcripts mapped to these rice planthopper SINE-like sequences (RPSlSs) were identified and appear to be transcriptionally regulated along the different developmental stages of planthoppers. Small RNAs derived from these RPSlSs are predominantly 26-28 nt long, which is the typical characteristic of PIWI-interacting RNAs. Phylogenetic analysis suggests that IIV6 might acquire a SINE-like retrotransposon from S. furcifera after the separation of the three rice planthoppers. This study provides further example of the horizontal transfer of an insect transposon to virus and suggests the association of rice planthoppers with iridoviruses in the past or present.IMPORTANCE This study provides an example of the horizontal transfer event from a rice planthopper genome to an invertebrate iridescent virus 6 (IIV-6, a iridovirus) genome. A small region of IIV-6 (∼300 nt) genome is highly homologous to the sequences presented in high copy numbers of three rice planthopper genomes that are related to the short interspersed nuclear elements (SINEs), a class of non-LTR retrotransposon (retroposon). The expression of these planthopper SINE-like sequences was confirmed and corresponding Piwi-interacting RNA-like small RNAs were identified and comprehensively characterized. Phylogenetic analysis suggests that the giant invertebrate iridovirus IIV-6 might obtain this SINE related sequence from Sogatella furcifera through an horizontal transfer event in the past. To the best of our knowledge, this is the first report of horizontal transfer event between a planthopper and a giant DNA virus, and also the first evidence for the eukaryotic origin of a genetic material in iridoviruses.

PMID:
30626674
DOI:
10.1128/JVI.01516-18
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