Global Analysis of the Transcriptional Response of Whitefly to
            <i>Tomato Yellow Leaf Curl China Virus</i>
            Reveals the Relationship of Coevolved Adaptations

Luan, Jing; Li, Junmin; Varela, Nélia; Wang, Yongliang; Li, Fangfang; Bao, Yan-Yuan; Zhang, Chuan‐Xi; Liu, Shu‐Sheng; Wang, Xiaowei

doi:10.1128/jvi.02507-10

Cited by 154 publications

(190 citation statements)

References 83 publications

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“…Furthermore, the persistent nonpropagative viruses do not replicate in their vectors; thus, they cannot trigger the siRNA antiviral pathway (50). It seems that immune-related responses such as autophagy and the synthesis of antimicrobial peptides could be activated by the infection of insect vectors by persistent nonpropagative viruses (50,51). The impact of insect immune systems on persistent infection by nonpropagative viruses is still poorly understood.…”

Section: Discussionmentioning

confidence: 99%

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Lan

Chen

Liu

et al. 2016

J Virol

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IMPORTANCE Many viral pathogens that cause significant global health and agricultural problems are transmitted via insect vectors. The first bottleneck in viral infection, the midgut epithelium, is a principal determinant of the ability of an insect species to transmit a virus. Southern rice black streaked dwarf virus (SRBSDV) is restricted exclusively to the midgut epithelium of an incompetent vector, the small brown planthopper (SBPH).Here, we show that silencing of the core component Dicer-2 of the small interfering RNA (siRNA) pathway increases viral titers in the midgut epithelium past the threshold (1.99 ؋ 10 9 copies of the SRBSDV P10 gene/g of midgut RNA) for viral dissemination into the midgut muscles and then into the salivary glands, allowing the SBPH to become a competent vector of SRBSDV. This result is the first evidence that the siRNA antiviral pathway has a direct role in the control of viral dissemination from the midgut epithelium and that it affects the competence of the virus's vector. Many viral pathogens that cause significant global health and agricultural problems are arthropod borne and transmitted via an insect vector. Many plant viruses are transmitted in a persistent manner by sap-sucking insects, including planthoppers, leafhoppers, thrips, and aphids (1-3). Plant viruses, when ingested by their insect vectors, establish their initial infection in the midgut epithelium, from where they disseminate to the midgut visceral muscles (1-3). The viruses then move from the midgut muscles into the hemolymph and finally into the salivary glands, from where they can be introduced into plant hosts (1-3). Efficient viral infection of the midgut epithelium, where initial infection is established, is thus a determinative factor in the ability of an insect species to transmit a certain plant virus.This ability of an insect species to transmit a virus, which has been described as vector competence, is common in nature (4, 5). For many years, the midgut barrier has been believed to be the principal determinant of vector competence (1-9). For example, infection of the incompetent insect vectors of Rice dwarf virus and SRBSDV, two plant reoviruses, and Tomato spotted wilt virus (TSWV), a tospovirus, is restricted to the midgut epithelium (7-10). The inability of incompetent insect vectors to transmit these viruses may be caused by a failure of the virus to efficiently replicate in or disseminate from the midgut epithelium (1-5). It is possible that viral titers in the midgut epithelium of incompetent vectors are unable to reach the threshold needed for viral dissemination. The innate immune response in the midgut epithelium may effectively control viral accumulation, thus blocking viral transmission by incompetent vectors. However, whether the initial antiviral immune pathway(s) in the insect midgut can modulate the competence of plant virus vectors is not unknown.Several mosquito and Drosophila innate immune responses have been reported to have an antiviral effect. These responses include RNA interfere...

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Section: Discussionmentioning

confidence: 99%

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Lan

Chen

Liu

et al. 2016

J Virol

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“…Along this pathway, begomoviruses must overcome several membrane barriers that incur close relationships between vector components and virus-encoded proteins (13,46). Previous research on begomoviruswhitefly interactions focused on parameters of virus acquisition, retention, and inoculation by whiteflies, and few attempts have been made to discover vector components and to unravel mechanisms that underlie these interactions (18,23,24,32,33,(47)(48)(49). Currently, only two heat shock proteins, BtHSP16 and BtHSP70, and a 63-kDa GroEL protein produced by secondary endosymbionts of B. tabaci have been implicated in direct interaction with the viral CP (22)(23)(24).…”

Section: Discussionmentioning

confidence: 99%

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Wei

Zhao

Zhang

et al. 2014

J Virol

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The majority of plant viruses are vectored by arthropods via persistent-circulative or noncirculative transmission. Previous studies have shown that specific binding sites for noncirculative viruses reside within the stylet or foregut of insect vectors, whereas the transmission mechanisms of circulative viruses remain ambiguous. Here we report the critical roles of whitefly primary salivary glands (PSGs) in the circulative transmission of two begomoviruses. The Middle East Asia Minor 1 (MEAM1) species of the whitefly Bemisia tabaci complex efficiently transmits both Tomato yellow leaf curl China virus (TYLCCNV) and Tomato yellow leaf curl virus (TYLCV), whereas the Mediterranean (MED) species transmits TYLCV but not TYLCCNV. PCR and fluorescence in situ hybridization experiments showed that TYLCCNV efficiently penetrates the PSGs of MEAM1 but not MED whiteflies. When a fragment of the coat protein of TYLCCNV was exchanged with that of TYLCV, mutated TYLCCNV accumulated in the PSGs of MED whiteflies, while mutant TYLCV was nearly undetectable. Confocal microscopy revealed that virion transport in PSGs follows specific paths to reach secretory cells in the central region, and the accumulation of virions in the secretory region of PSGs was correlated with successful virus transmission. Our findings demonstrate that whitefly PSGs, in particular the cells around the secretory region, control the specificity of begomovirus transmission. IMPORTANCEOver 75% of plant viruses are transmitted by insects. However, the mechanisms of virus transmission by insect vectors remain largely unknown. Begomoviruses and whiteflies are a complex of viruses and vectors which threaten many crops worldwide. We investigated the transmission of two begomoviruses by two whitefly species. We show that specific cells of the whitefly primary salivary glands control viral transmission specificity and that virion transport in the glands follows specific paths to reach secretory cells in the central region and then to reach the salivary duct. Our results indicate that the secretory cells in the central region of primary salivary glands determine the recognition and transmission of begomoviruses. These findings set a foundation for future research not only on circulative plant virus transmission but also on other human and animal viruses transmitted by arthropod vectors.

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“…Below a particular threshold, few vectors ingesting the blood meal become infected; above this threshold, significant numbers become infected (4). At the molecular level, transcriptional profiling of disparate insects challenged orally by viral pathogens suggest that there is an active immune response that includes the induction or down-regulation of many known insect immune pathways such as the JAK/ STAT, Toll, and JNK signaling (7)(8)(9). However, less is known about whether the induction of these pathways have a direct role in viral restriction in the gut epithelium and whether there are additional pathways that play important roles in barrier immunity.…”

mentioning

confidence: 99%

ERK signaling couples nutrient status to antiviral defense in the insect gut

Hopkins

Sabin

et al. 2013

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

127

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A unique facet of arthropod-borne virus (arbovirus) infection is that the pathogens are orally acquired by an insect vector during the taking of a blood meal, which directly links nutrient acquisition and pathogen challenge. We show that the nutrient responsive ERK pathway is both induced by and restricts disparate arboviruses in Drosophila intestines, providing insight into the molecular determinants of the antiviral "midgut barrier." Wild-type flies are refractory to oral infection by arboviruses, including Sindbis virus and vesicular stomatitis virus, but this innate restriction can be overcome chemically by oral administration of an ERK pathway inhibitor or genetically via the specific loss of ERK in Drosophila intestinal epithelial cells. In addition, we found that vertebrate insulin, which activates ERK in the mosquito gut during a blood meal, restricts viral infection in Drosophila cells and against viral invasion of the insect gut epithelium. We find that ERK's antiviral signaling activity is likely conserved in Aedes mosquitoes, because genetic or pharmacologic manipulation of the ERK pathway affects viral infection of mosquito cells. These studies demonstrate that ERK signaling has a broadly antiviral role in insects and suggest that insects take advantage of cross-species signals in the meal to trigger antiviral immunity.innate immunity | enterocytes

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Global Analysis of the Transcriptional Response of Whitefly to Tomato Yellow Leaf Curl China Virus Reveals the Relationship of Coevolved Adaptations

Cited by 154 publications

References 83 publications

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

ERK signaling couples nutrient status to antiviral defense in the insect gut

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