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. 2021 Jan 8:11:621141.
doi: 10.3389/fmicb.2020.621141. eCollection 2020.

A Novel Iflavirus Was Discovered in Green Rice Leafhopper Nephotettix cincticeps and Its Proliferation Was Inhibited by Infection of Rice Dwarf Virus

Wenxi Jia  1 , Fei Wang  1 , Jingjing Li  1   2 , Xuefei Chang  1 , Yi Yang  1 , Hongwei Yao  1 , Yanyuan Bao  1 , Qisheng Song  2 , Gongyin Ye  1
Affiliations

A Novel Iflavirus Was Discovered in Green Rice Leafhopper Nephotettix cincticeps and Its Proliferation Was Inhibited by Infection of Rice Dwarf Virus

Wenxi Jia et al. Front Microbiol. .

Abstract

The green rice leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae), is a key insect vector transmitting rice dwarf virus (RDV) that causes rice dwarf disease. We discovered a novel iflavirus from the transcriptomes of N. cincticeps and named it as Nephotettix cincticeps positive-stranded RNA virus-1 (NcPSRV-1). The viral genome consists of 10,524 nucleotides excluding the poly(A) tail and contains one predicted open reading frame encoding a polyprotein of 3,192 amino acids, flanked by 5' and 3' untranslated regions. NcPSRV-1 has a typical iflavirus genome arrangement and is clustered with the members of the family Iflaviridae in the phylogenetic analysis. NcPSRV-1 was detected in all tested tissues and life stages of N. cincticeps and could be transmitted horizontally and vertically. Moreover, NcPSRV-1 had high prevalence in the laboratory populations and was widely spread in field populations of N. cincticeps. NcPSRV-1 could also infect the two-striped leafhopper, Nephotettix apicalis, at a 3.33% infection rate, but was absent in the zigzag leafhopper, Recilia dorsalis, and rice Oryza sativa variety TN1. The infection of RDV altered the viral load and infection rate of NcPSRV-1 in N. cincticeps, for which it seems that RDV has an antagonistic effect on NcPSRV-1 infection in the host.

Keywords: Iflaviridae; Nephotettix cincticeps; co-infection; covert infection; distribution; rice dwarf virus; transmission; virus-virus interaction.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Analyses of NcPSRV-1. (A) Genome organization of NcPSRV-1. NcPSRV-1 genome encodes one polyprotein with the structural proteins VP1–VP4 (capsid proteins) located in the N-terminal region and the non-structural proteins responsible for replication and morphogenesis, helicase (Hel), protease (Pro), and RNA-dependent RNA polymerase (RdRp) in the C-terminal region. The open reading frame is flanked by 5' and 3' untranslated regions (UTRs), both contain secondary RNA structures. The viral genome-linked protein (VPg) is expected to link covalently to the 5' end of the genome and a leader protein (L) is also expected before the VP2 protein. (B) Phylogenetic analysis of NcPSRV-1. The phylogenetic tree was constructed based on the deduced RNA-dependent RNA polymerase domain. Viruses are from the order Picornavirales and the Genbank accession numbers are shown in each node. The sizes of the circles positioned on the branches represent the bootstrap values as percentages calculated from 1,000 replicates. NcPSRV-1 is shown in bold and indicated with an arrow.
Figure 2
Figure 2
Alignment of the predicted cleavage sites of VP4-VP3 proteins of NcPSRV-1 among the iflaviruses. The amino acids shaded in orange and blue indicate the conservative and similar residues, respectively. The expected cleavage site is marked with an arrowhead. Numbers in the left of the sequences refer to the amino acid positions from the N-terminus of the viral polyprotein. The viral abbreviations and accession numbers are listed in Supplementary Table S2.
Figure 3
Figure 3
Tissue and developmental expression patterns of NcPSRV-1 in N. cincticeps. (A) The viral loads of NcPSRV-1 in N. cincticeps in brain, salivary gland, midgut, fat body, carcass, ovary and testis. (B) The viral loads of NcPSRV-1 of N. cincticeps in eggs, 1st-5th instar nymphs and adults (males and females). Data represent means ± standard errors (SEM; n = 3). Bars annotated with the same letters are not significantly different (p < 0.05, Tukey’s multiple comparison test).
Figure 4
Figure 4
Prevalence of NcPSRV-1 in different geographical regions. Ten N. cincticeps field populations were collected from different geographical regions in China. The NcPSRV-1 infection rate of each population is shown (n ≥ 38).
Figure 5
Figure 5
Viral loads of NcPSRV-1 in laboratory populations. The viral loads of population A in 2017–2020 are shown individually. Each spot represents the value for an individual. The average viral levels of population A in each year represent means ± SEM (n ≥ 46). Statistical significance is indicated by asterisks (* p < 0.05, *** p < 0.001, Student’s t-test).
Figure 6
Figure 6
Detection of NcPSRV-1 in the honeydew of viruliferous N. cincticeps. NcPSRV-1 was detected via PCR by using two pairs of specific primers NcPSRV-6F/NcPSRV-6R and NcPSRV-15F/NcPSRV-15R. In lanes 1 and 3, the cDNA sample from the honeydew used for PCR was diluted 10 times. The cDNA sample used in lanes 2 and 4 was not diluted.
Figure 7
Figure 7
Viral loads of NcPSRV-1 in N. cincticeps eggs. (A) The viral loads of NcPSRV-1 in sodium hypochlorite-treated eggs and non-treated eggs. (B) The viral loads of NcPSRV-1 in the eggs with red eyespot (7 days after oviposition) and without red eyespot (3 days after oviposition). Means ± SEM (n = 3). Statistical significance is indicated by asterisks (* p < 0.05, Student’s t-test).
Figure 8
Figure 8
Viral loads of NcPSRV-1 in the rice dwarf virus (RDV)-feeding and non-feeding N. cincticeps populations. Each spot represents the value for an individual. The average viral levels of population B (n = 50) and C (n = 42) represent means ± SEM. Statistical significance is indicated by asterisks (*** p < 0.001, Student’s t-test).
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