Synergism Between Southern rice black-streaked dwarf virus and Rice ragged stunt virus Enhances Their Insect Vector Acquisition

Southern rice black-streaked dwarf virus (SRBSDV), a tentative species in the genus Fijivirus, family Reoviridae, is a novel rice virus transmitted by the white-backed planthopper (Sogatella furcifera). Since its discovery in 2001, SRBSDV has spread rapidly throughout eastern and southeastern Asia and caused large rice losses in China and Vietnam. Rice ragged stunt virus (RRSV) (genus Oryzavirus, family Reoviridae) is a common rice virus vectored by the brown planthopper (Nilaparvata lugens). RRSV is also widely distributed in eastern and southeastern Asia but has not previously caused serious problems in China owing to its low incidence. With SRBSDV's spread, however, RRSV has become increasingly common in China, and is frequently found in co-infection with SRBSDV. In this study, we show that SRBSDV and RRSV interact synergistically, the first example of synergism between plant viruses in the family Reoviridae. Rice plants co-infected with both viruses displayed enhanced stunting, earlier symptoms, and higher virus titers compared with singly infected plants. Furthermore, white-backed and brown planthoppers acquired SRBSDV and RRSV, respectively, from co-infected plants at higher rates. We propose that increased RRSV incidence in Chinese fields is partly due to synergism between SRBSDV and RRSV.

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Southern rice black-streaked dwarf virus Alters Insect Vectors' Host Orientation Preferences to Enhance Spread and Increase Rice ragged stunt virus Co-Infection

Phytopathology ◽

10.1094/phyto-08-13-0227-r ◽

2014 ◽

Vol 104 (2) ◽

pp. 196-201 ◽

Cited By ~ 49

Author(s):

Han Wang ◽

Donglin Xu ◽

Lingling Pu ◽

Guohui Zhou

Keyword(s):

Host Preference ◽

Southern China ◽

Brown Planthopper ◽

Nilaparvata Lugens ◽

Plant Viruses ◽

Dwarf Virus ◽

Virus Spread ◽

Sogatella Furcifera ◽

Rice Plants ◽

Rice Ragged Stunt Virus

In recent years, Southern rice black-streaked dwarf virus (SRBSDV), a tentative species in the genus Fijivirus (family Reoviridae), has spread rapidly and caused serious rice losses in eastern and southeastern Asia. With this virus spread, Rice ragged stunt virus (RRSV, genus Oryzavirus, family Reoviridae) became more common in southern China, usually in co-infection with the former. SRBSDV and RRSV are transmitted by two different species of planthoppers, white-backed planthopper (WBPH, Sogatella furcifera) and brown planthopper (BPH, Nilaparvata lugens), respectively, in a persistent, circulative, propagative manner. In this study, using a Y-shape olfactometer-based device, we tested the host preference of three types of macropterous WBPH adults for healthy or SRBSDV-infected rice plants. The results showed that virus-free WBPHs significantly preferred infected rice plants to healthy plants, whereas both the viruliferous and nonviruliferous WBPHs preferred healthy plants to infected plants. In additional tests, we found that the BPHs significantly preferred healthy plants when they were virus free, whereas RRSV-carrying BPHs preferred SRBSDV-infected rice plants. From these findings, we propose that plant viruses may alter host selection preference of vectors to enhance their spread and that of insects vectoring another virus to result in co-infection with more than one virus.

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Interplay of Rice Stripe Virus and Rice Black Streaked Dwarf Virus during Their Acquisition and Accumulation in Insect Vector

Viruses ◽

10.3390/v13061121 ◽

2021 ◽

Vol 13 (6) ◽

pp. 1121

Author(s):

Marcia Beatriz Moya Fernández ◽

Wenwen Liu ◽

Lu Zhang ◽

Jamal-U-Ddin Hajano ◽

Xifeng Wang

Keyword(s):

Epithelial Cells ◽

Crop Production ◽

Brown Planthopper ◽

Rice Stripe Virus ◽

Plant Viruses ◽

Dwarf Virus ◽

Insect Vector ◽

Laodelphax Striatellus ◽

Persistent Viruses ◽

Vector Insect

Plant viruses transmitted by hemipteran vectors commonly cause losses to crop production. Rice stripe virus (RSV) and rice black streaked dwarf virus (RBSDV) are transmitted to rice plants by the same vector, the small brown planthopper (SBPH), Laodelphax striatellus Fallén, in a persistent propagative manner. However, rarely do the respective diseases they cause occur simultaneously in a field. Here, we determined the acquisition efficiency of RSV and RBSDV when acquired in succession or simultaneously by SBPH. When RBSDV was acquired first, RSV acquisition efficiency was significantly lower than when only acquiring RSV. However, RBSDV acquisition efficiency from insects that acquired RSV first was not significantly different between the insects only acquiring RBSDV. Immunofluorescence assays showed that the acquisition of RBSDV first might inhibit RSV entry into midgut epithelial cells, but RSV did not affect RBSDV entry. SBPHs were more likely to acquire RBSDV when they were feeding on plants coinfected with the two viruses. When RBSDV was acquired before RSV, RBSDV titer was significantly higher and RSV titer first declined, then increased compared to when only acquiring RBSDV or RSV. Only 5% of the SBPHs acquired both viruses when feeding on plants coinfected with RSV and RBSDV. These results provide a better understanding of the interaction between two persistent viruses when present in the same vector insect and explain why RSV and RBSDV occur in intermittent epidemics.

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Insecticide Susceptibility and Wing-Form Ratio of the Brown Planthopper, Nilaparvata lugens (STÅL) (Hemiptera : Delphacidae) and the White Backed Planthopper, Sogatella furcifera (HORVATH) (Hemiptera : Delphacidae) of Southeast Asia

Applied Entomology and Zoology ◽

10.1303/aez.15.10 ◽

1980 ◽

Vol 15 (1) ◽

pp. 10-19 ◽

Cited By ~ 31

Author(s):

Toru NAGATA ◽

Takeo MASUDA

Keyword(s):

Southeast Asia ◽

Brown Planthopper ◽

Nilaparvata Lugens ◽

Sogatella Furcifera ◽

Wing Form ◽

Insecticide Susceptibility

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Ketahanan padi (Oryza sativa L.) varietas IPB 3S terhadap wereng batang cokelat (Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)

Jurnal Entomologi Indonesia ◽

10.5994/jei.17.2.97 ◽

2020 ◽

Vol 17 (2) ◽

pp. 97

Author(s):

Andi Nurdaaniyah ◽

Dadang Dadang ◽

I Wayan Winasa

Keyword(s):

Sex Ratio ◽

Insect Pests ◽

Oryza Sativa L ◽

Feeding Activity ◽

Brown Planthopper ◽

Nilaparvata Lugens ◽

Population Increase ◽

Rice Varieties ◽

High Loss ◽

Rice Plants

Brown planthopper (Nilaparvata lugens (Stål)) is one of the major rice insect pests that is known to cause high loss of rice production. One of the strategies to control this pest is by using resistant rice varieties. The aim of this research was to study the resistance of IPB 3S variety to BPH by measuring BPH fecundity, sex ratio, feeding activity as well as population increase compared to Ciherang variety against brown planthopper (N. lugens). Fecundity test used a pair of BPH adult infested on 21 days after planting (DAP) of rice plants. Eggs laid in rice stalks and the rest of eggs in the ovary were counted. In order to know the change of sex ratio, a pair of BPH adults was infested on 30 DAP rice plants and allowed to lay eggs. The calculation of sex ratio was conducted at adult stage of BPH by segregation between male and female adults. Feeding activity of BPH was evaluated using ninhydrin and analyzed qualitatively using spectrophotometer. Ten fourth instar nymphs of BPH was infested on 30 DAP old of rice seedlings. Honeydew secreted by BPH was collected to filter paper sprayed with ninhydrin. Population increased test was conducted by infesting five pairs of BPH adults on 35 DAP old rice plants. Observations was conducted on nymph and adult stages. Each test was replicated 10 times. In general, IPB 3S is slightly resistant to BPH, compared to Ciherang variety. The feeding activity of BPH is higher in Ciherang compared to IPB3S. However, the fecundity and population increased of BPH in Ciherang is similar to IPB3S.

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Stable Establishment of Cardinium spp. in the Brown Planthopper Nilaparvata lugens despite Decreased Host Fitness

Applied and Environmental Microbiology ◽

10.1128/aem.02509-19 ◽

2019 ◽

Vol 86 (4) ◽

Author(s):

Tong-Pu Li ◽

Chun-Ying Zhou ◽

Si-Si Zha ◽

Jun-Tao Gong ◽

Zhiyong Xi ◽

...

Keyword(s):

Cytoplasmic Incompatibility ◽

Developmental Stages ◽

Brown Planthopper ◽

Nilaparvata Lugens ◽

Hatching Rate ◽

Wild Populations ◽

Maternal Transmission ◽

Sogatella Furcifera ◽

Content Type ◽

Major Pest

ABSTRACT The brown planthopper Nilaparvata lugens (Hemiptera) is a major pest of rice crops in Asia. Artificial transinfections of Wolbachia have recently been used for reducing host impacts, but transinfections have not yet been undertaken with another important endosymbiont, Cardinium. This endosymbiont can manipulate the reproduction of hosts through phenotypes such as cytoplasmic incompatibility (CI), which is strong in the related white-backed planthopper, Sogatella furcifera (Hemiptera). Here, we stably infected N. lugens with Cardinium from S. furcifera and showed that it exhibits perfect maternal transmission in N. lugens. The density of Cardinium varied across developmental stages and tissues of the transinfected host. Cardinium did not induce strong CI in N. lugens, likely due to its low density in testicles. The infection did decrease fecundity and hatching rate in the transinfected host, but a decrease in fecundity was not apparent when transinfected females mated with Wolbachia-infected males. The experiments show the feasibility of transferring Cardinium endosymbionts across hosts, but the deleterious effects of Cardinium on N. lugens limit its potential to spread in wild populations of N. lugens in the absence of strong CI. IMPORTANCE In this study we established a Cardinium-infected N. lugens line that possessed complete maternal transmission. Cardinium had a widespread distribution in tissues of N. lugens, and this infection decreased the fecundity and hatching rate of the host. Our findings emphasize the feasibility of transinfection of Cardinium in insects, which expands the range of endosymbionts that could be manipulated for pest control.

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Rice black-streaked dwarf virus P10 suppresses protein kinase C in insect vector through changing the subcellular localization of LsRACK1

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2018.0315 ◽

2019 ◽

Vol 374 (1767) ◽

pp. 20180315 ◽

Cited By ~ 3

Author(s):

Lina Lu ◽

Qi Wang ◽

Deqing Huang ◽

Qiufang Xu ◽

Xueping Zhou ◽

...

Keyword(s):

Protein Kinase C ◽

Protein Kinase ◽

Subcellular Localization ◽

Fluorescent Protein ◽

Brown Planthopper ◽

Subcellular Fractionation ◽

Dwarf Virus ◽

Insect Vector ◽

Kinase C ◽

Green Fluorescent

Rice black-streaked dwarf virus (RBSDV) was known to be transmitted by the small brown planthopper (SBPH) in a persistent, circulative and propagative manner in nature. Here, we show that RBSDV major outer capsid protein (also known as P10) suppresses the protein kinase C (PKC) activity of SBPH through interacting with the receptor for activated protein kinase C 1 (LsRACK1). The N terminal of P10 (amino acids (aa) 1–270) and C terminal of LsRACK1 (aa 268–315) were mapped as crucial for the interaction. Confocal microscopy and subcellular fractionation showed that RBSDV P10 fused to enhanced green fluorescent protein formed vesicular structures associated with endoplasmic reticulum (ER) membranes in Spodoptera frugiperda nine cells. Our results also indicated that RBSDV P10 retargeted the initial subcellular localization of LsRACK1 from cytoplasm and cell membrane to ER and affected the function of LsRACKs to activate PKC. Inhibition of RACK1 by double stranded RNA-induced gene silencing significantly promoted the replication of RBSDV in SBPH. In addition, the PKC pathway participates in the antivirus innate immune response of SBPH. This study highlights that RACK1 negatively regulates the accumulation of RBSDV in SBPH through activating the PKC signalling pathway, and RBSDV P10 changes the subcellular localization of LsRACK1 and affects its function to activate PKC. This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.

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