Transovarial Transmission of a Plant Virus Is Mediated by Vitellogenin of Its Insect Vector

Huo, Yan; Liu, Wenwen; Zhang, Fujie; Chen, Xiaoying; Li, Li; Liu, Qifei; Zhou, Yijun; Wèi, Tàiyún; Fang, Rongxiang; Wang, Xifeng

doi:10.1371/journal.ppat.1003949

Cited by 129 publications

(157 citation statements)

References 48 publications

(52 reference statements)

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“…Transovarial transmission of plant viruses has received constant attention since 1933 (5-7). However, most of the reports were focused on circulative-propagative plant viruses, such as reoviruses, rhabdoviruses, or tenuiviruses (31)(32)(33)(34). Even so, some research groups have investigated the transovarial transmission of circulative-nonpropagative begomoviruses in the past 50 y.…”

Section: Discussionmentioning

confidence: 99%

“…To identify the essential amino acids that are responsible for transovarial transmission, more virus CP mutants with single-amino acid substitution could be generated to test their transovarial transmission and interactions with Vg. Previous study has shown that the transovarial transmission of a propagative RNA virus (Rice stripe virus) is mediated by Vg of its insect vector (31). Moreover, the Babesia parasite in Haemaphysaalis longicornis and the ZAM virus in Drosophila melanogaster are dependent on the Vg receptor when transmitted into the oocyte (45,46).…”

Section: Discussionmentioning

confidence: 99%

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Vector development and vitellogenin determine the transovarial transmission of begomoviruses

Wei

Guo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

107

114

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The majority of plant viruses are transmitted by insect vectors between hosts, and transovarial transmission of viruses from vector parents to offspring has great significance to their epidemiology. Begomoviruses are transmitted by the whitefly Bemisia tabaci in a circulative manner and are maintained through a plantinsect-plant cycle. Other routes of begomovirus transmission are not clearly known. Here, we report that transovarial transmission from female whiteflies to offspring often happens for one begomovirus, Tomato yellow leaf curl virus (TYLCV), and may have contributed significantly to its global spread. We found that TYLCV entry of the reproductive organ of its vector mainly depended on the developmental stage of the whitefly ovary, and the transovarial transmission of TYLCV to offspring increased with whitefly adult age. The specific interaction between virus coat protein (CP) and whitefly vitellogenin (Vg) was vital for virus entry into whitefly ovary. When knocking down the expression of Vg, the entry of TYLCV into ovary was inhibited and the transovarial transmission efficiency decreased. In contrast, another begomovirus, Papaya leaf curl China virus (PaLCuCNV), CP did not interact with whitefly Vg, and PaLCuCNV could not be transovarially transmitted by whiteflies. We further showed that TYLCV could be maintained for at least two generations in the absence of virusinfected plants, and the adult progenies were able to infect healthy plants in both the laboratory and field. This study reports the transovarial transmission mechanism of begomoviruses, and it may help to explain the evolution and global spread of some begomoviruses.begomovirus | transovarial transmission | vector development | vitellogenin | whitefly

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Vector development and vitellogenin determine the transovarial transmission of begomoviruses

Wei

Guo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

107

114

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“…RSV-free and viruliferous insects (Laodelphax striatellus) were obtained and maintained as described previously (Huo et al, 2014). RSV inoculation was performed as described previously (Satoh et al, 2010).…”

Section: Plant Growth and Rsv Infectionmentioning

confidence: 99%

“…Total protein was separated on an SDS-PAGE gel and transferred electrophoretically to polyvinylidene difluoride membranes (Amersham Bioscience), which were incubated with purified polyclonal antibodies (antiOsMADS23, anti-OsMADS27a, anti-OsMADS57 [BGI], and anti-CP [Huo et al, 2014]) to determine protein accumulation.…”

Section: Western-blot Analysismentioning

confidence: 99%

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

et al. 2016

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Plant RNA-DEPENDENT RNA POLYMERASE1 (RDR1) is a key component of the antiviral RNA-silencing pathway, contributing to the biogenesis of virus-derived small interfering RNAs. This enzyme also is responsible for producing virusactivated endogenous small interfering RNAs to stimulate the broad-spectrum antiviral activity through silencing host genes. The expression of RDR1 orthologs in various plants is usually induced by virus infection. However, the molecular mechanisms of activation of RDR1 expression in response to virus infection remain unknown. Here, we show that a monocot-specific microRNA, miR444, is a key factor in relaying the antiviral signaling from virus infection to OsRDR1 expression. The expression of miR444 is enhanced by infection with Rice stripe virus (RSV), and overexpression of miR444 improves rice (Oryza sativa) resistance against RSV infection accompanied by the up-regulation of OsRDR1 expression. We further show that three miR444 targets, the MIKC C -type MADS box proteins OsMADS23, OsMADS27a, and OsMADS57, form homodimers and heterodimers between them to repress the expression of OsRDR1 by directly binding to the CArG motifs of its promoter. Consequently, an increased level of miR444 diminishes the repressive roles of OsMADS23, OsMADS27a, and OsMADS57 on OsRDR1 transcription, thus activating the OsRDR1-dependent antiviral RNA-silencing pathway. We also show that overexpression of miR444-resistant OsMADS57 reduced OsRDR1 expression and rice resistance against RSV infection, and knockout of OsRDR1 reduced rice resistance against RSV infection. In conclusion, our results reveal a molecular cascade in the rice antiviral pathway in which miR444 and its MADS box targets directly control OsRDR1 transcription.RNA silencing mediated by regulatory small RNAs (microRNAs [miRNAs] and small interfering RNAs [siRNAs]) negatively regulates gene expression at the posttranscriptional level or at the transcriptional level in eukaryotic organisms. Besides small RNAs, plant RNA-silencing pathways incorporate several kinds of core protein components, such as DICER-LIKE (DCL) RNase III endonucleases, which process long doublestranded RNA (dsRNA) into small RNA duplexes; ARGONAUTEs (AGOs), the major effector of the RNA-induced silencing complexes, which bind to small RNAs for silencing target RNAs; and RNA-dependent RNA polymerases (RDRs), which are required for copying single-stranded RNAs into dsRNAs for downstream processing by DCLs. Multiple DCLs, AGOs, and RDRs have evolved in plants and thus form an array of RNA-silencing pathways (Axtell, 2013;Martínez de Alba et al., 2013;Bologna and Voinnet, 2014). Among them, the antiviral RNA-silencing pathway is the earliest described and most extensively studied. It is well known that the antiviral silencing pathway directly targets viral RNAs. Briefly, as in Arabidopsis (Arabidopsis thaliana), the stem-loop structures and dsRNA replication intermediates of viral RNAs are recognized and cleaved by DCLs (DCL4 and DCL2) to produce primary virus-derived small interferi...

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“…Insect proteins are expected to play a role as virus receptors, in the uptake and transport of virus through various tissues, and in replication of the viruses (1,3,14). In our recent study, vitellogenin of Laodelphax striatellus (small brown planthopper) was demonstrated to play a critical role in transovarial transmission of Rice stripe virus (RSV) (15). Diverse proteins of Sogatella furcifera (white-backed planthopper) have also been identified as acting in the successful transmission of southern rice black-streaked dwarf virus (16).…”

mentioning

confidence: 99%

Proteomic Analysis of Interaction between a Plant Virus and Its Vector Insect Reveals New Functions of Hemipteran Cuticular Protein

Liu

Gray

Huo

et al. 2015

Molecular & Cellular Proteomics

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Numerous viruses can be transmitted by their corresponding vector insects; however, the molecular mechanisms enabling virus transmission by vector insects have been poorly understood, especially the identity of vector components interacting with the virus. Here, we used the yeast two-hybrid system to study proteomic interactions of a plant virus (Rice stripe virus, RSV, genus Tenuivirus) with its vector insect, small brown planthopper (Laodelphax striatellus). Sixty-six proteins of L. striatellus that interacted with the nucleocapsid protein (pc3) of RSV were identified. A virus-insect interaction network, constructed for pc3 and 29 protein homologs of Drosophila melanogaster, suggested that nine proteins might directly interact with pc3. Of the 66 proteins, five (atlasin, a novel cuticular protein, jagunal, NAC domain protein, and vitellogenin) were most likely to be involved in viral movement, replication, and transovarial transmission. This work also provides evidence that the novel cuticular protein, CPR1, from L. striatellus is essential for RSV transmission by its vector insect. CPR1 binds the nucleocapsid protein (pc3) of RSV both in vivo and in vitro and colocalizes with RSV in the hemocytes of L. striatellus. Knockdown of CPR1 transcription using RNA interference resulted in a decrease in the concentration of RSV in the hemolymph, salivary glands and in viral transmission efficiency. These data suggest that CPR1 binds RSV in the insect and stabilizes the viral concentration in the hemolymph, perhaps to protect the virus or to help move the virus to the salivary tissues. Our studies provide direct experimental evidence that viruses can use existing vector proteins to aid their survival in the hemolymph. Identifying these pu-

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Transovarial Transmission of a Plant Virus Is Mediated by Vitellogenin of Its Insect Vector

Cited by 129 publications

References 48 publications

Vector development and vitellogenin determine the transovarial transmission of begomoviruses

Vector development and vitellogenin determine the transovarial transmission of begomoviruses

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

Proteomic Analysis of Interaction between a Plant Virus and Its Vector Insect Reveals New Functions of Hemipteran Cuticular Protein

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