A plant DNA virus replicates in the salivary glands of its insect vector via recruitment of host DNA synthesis machinery

He, Ya-Zhou; Wang, Yumeng; Yin, Tian-Yan; Fiallo‐Olivé, Elvira; Liu, Yin-Quan; Hanley‐Bowdoin, Linda; Wang, Xiaowei

doi:10.1073/pnas.1820132117

Cited by 79 publications

(80 citation statements)

References 52 publications

(105 reference statements)

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“…In addition, circumstantial evidence of TYLCV replication is provided by the successful transovarial transmission of the virus from one generation to the next of the whitefly vector ( 11 – 14 ). Equally important, case studies also showed that both replication and transovarial transmission of TYLCV in whiteflies may be conditional and intermittent ( 13 , 14 ), and the replication of TYLCV occurs mainly in the salivary glands of the whitefly vector ( 15 ).…”

Section: Introductionmentioning

confidence: 99%

Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

Wang

Ban

et al. 2020

mSystems

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Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci. Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo. Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission. IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.

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Section: Introductionmentioning

confidence: 99%

Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

Wang

Ban

et al. 2020

mSystems

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“…It is tempting to speculate whether it can alter the insect cell cycle and induce an endoreplication cycle as in plants or has evolved alternate strategies in the insect. Not all begomoviruses appear to replicate in the whitefly [37], and hence additional efforts are needed to understand why only certain virus species replicate within the insect. The continuous virus replication might not be beneficial to the viruses, because this can induce insect autophagy and antimicrobial peptide production leading to virion destruction and the inhibition of prolonged virus replication [38].…”

Section: The Voyage Of Virus Inside the Insect Vectormentioning

confidence: 99%

“…The continuous virus replication might not be beneficial to the viruses, because this can induce insect autophagy and antimicrobial peptide production leading to virion destruction and the inhibition of prolonged virus replication [38]. The active viral gene transcription of some begomoviruses can occur within the insect [37][38][39]. Strikingly, an insect transcription factor promotes viral gene transcription by binding to a CACGTG motif at the IR of a begomovirus [40].…”

Section: The Voyage Of Virus Inside the Insect Vectormentioning

confidence: 99%

Plant-virus-insect tritrophic interactions: insights into the functions of geminivirus virion-sense strand genes

Kumar

Shivaprasad

2020

Proc. R. Soc. B.

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The genome of the plant-infecting viruses in the family Geminiviridae is composed of one or two circular single stranded DNA of approximately 2.7–5.2 kb in length. These viruses have emerged as the most devastating pathogen infecting a large number of crops and weeds across the continents. They code for fewer open reading frames (ORFs) through the generation of overlapping transcripts derived from the bidirectional viral promoters. Members of geminiviruses code for up to four ORFs in the virion-sense strand, and their gene expression is regulated by various cis -elements located at their promoters in the intergenic region. These viral proteins perform multiple functions at every stage of the viral life cycle such as virus transport, insect-mediated virus transmission and suppression of host defence. They impede the host's multi-layered antiviral mechanisms including gene silencing (at transcriptional and post-transcriptional levels) and hypersensitive response. This review summarizes the essential role of virion-sense strand encoded proteins in transport of viral genomes within and between plant cells, countering defence in hosts (both plants and the insects), and also in the ubiquitous role in vector-mediated transmission. We highlight the significance of their pro-viral activities in manipulating host-derived innate immune responses and the interaction with whitefly-derived proteins. We also discuss the current knowledge on virus replication and transcription within the insect body.

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“…Taken together, these results suggest that DNA polymerase α is essential for the initial synthesis of the viral complementary strand, and therefore for the generation of the dsDNA replicative intermediate, while DNA polymerase δ, alone or in combination with α, is required for the following RCR. Interestingly, TYLCV has been recently proven to replicate in the insect vector in a DNA polymerase δ-dependent manner (He et al, 2020), which raises the idea that the mechanisms replicating geminiviruses might be conserved between the animal and plant kingdoms.…”

Section: Main Textmentioning

confidence: 99%

Plant DNA polymerases alpha and delta mediate replication of geminiviruses

Hua

Tan

et al. 2020

Preprint

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Geminiviruses are causal agents of devastating diseases in crops. Geminiviruses have circular single-stranded (ss)DNA genomes that are replicated in the nucleus of the infected plant cell through double-stranded (ds)DNA intermediates by the plant’s DNA replication machinery; which host DNA polymerase mediates geminiviral multiplication, however, has so far remained elusive. Here, we show that subunits of the nuclear replicative DNA polymerases α and δ physically interact with the geminivirus-encoded replication enhancer protein, C3, and are required for viral replication. Our results suggest that while DNA polymerase α is essential to generate the viral dsDNA intermediate, DNA polymerase δ mediates the synthesis of new copies of the geminiviral ssDNA genome, and that the virus-encoded C3 acts selectively recruiting DNA polymerase δ over ε to favour a productive replication.

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A plant DNA virus replicates in the salivary glands of its insect vector via recruitment of host DNA synthesis machinery

Cited by 79 publications

References 52 publications

Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

Plant-virus-insect tritrophic interactions: insights into the functions of geminivirus virion-sense strand genes

Plant DNA polymerases alpha and delta mediate replication of geminiviruses

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