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

Ya-Zhou He,Yu-Meng Wang,Tian-Yan Yin,Elvira Fiallo-Olivé,Yin-Quan Liu,Linda Hanley-Bowdoin,Xiao-Wei Wang

doi:10.1073/pnas.1820132117

Abstract

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses. So far, only some plant RNA viruses have been demonstrated to replicate in insect vectors and plant hosts. How plant viruses evolved to replicate in the animal kingdom remains largely unknown. Geminiviruses comprise a large family of plant-infecting, single-stranded DNA viruses that cause serious crop losses worldwide. Here, we report evidence and insight into the replication of the geminivirus tomato yellow leaf curl virus (TYLCV) in the whitefly (Bemisia tabaci) vector and that replication is mainly in the salivary glands. We found that TYLCV induces DNA synthesis machinery, proliferating cell nuclear antigen (PCNA) and DNA polymerase δ (Polδ), to establish a replication-competent environment in whiteflies. TYLCV replication-associated protein (Rep) interacts with whitefly PCNA, which recruits DNA Polδ for virus replication. In contrast, another geminivirus, papaya leaf curl China virus (PaLCuCNV), does not replicate in the whitefly vector. PaLCuCNV does not induce DNA-synthesis machinery, and the Rep does not interact with whitefly PCNA. Our findings reveal important mechanisms by which a plant DNA virus replicates across the kingdom barrier in an insect and may help to explain the global spread of this devastating pathogen.

Highlights

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses
We demonstrated transovarial transmission of tomato yellow leaf curl virus (TYLCV) in Middle East Asia Minor 1 (MEAM1) whiteflies and that all developmental stages of their progeny accumulate the virus efficiently (68 to 92%), and that adult offspring are able to transmit TYLCV to tomato plants [24]. Given that this type of transmission usually indicates that the virus is replicating in the vector, we examined the dynamics of TYLCV in whole bodies of first-generation (F1) adults, which developed from eggs deposited on cotton by viruliferous MEAM1 whiteflies
Alterations to whitefly biology, and accumulation of viral DNA and transcripts in the vector have been proposed as evidence of replication of TYLCV in the whitefly vector [17,18,19,20,21]

Summary

Introduction

Whereas most of the arthropod-borne animal viruses replicate in their vectors, this is less common for plant viruses. TYLCV replication-associated protein (Rep) interacts with whitefly PCNA, which recruits DNA Polδ for virus replication. Another geminivirus, papaya leaf curl China virus (PaLCuCNV), does not replicate in the whitefly vector. Used by plant viruses to cross the kingdom barrier to replicate within insect vectors have rarely been reported This question is of major importance because knowledge of host expansion will give a better understanding of virus evolution, and identification of virus and vector components involved in replication could lead to new strategies to interdict virus spread. Complex interactions occur between virus-encoded proteins and Many viruses, including those that cause significant global problems in humans, animals, and plants, rely on arthropod vectors to move from one host to another [1, 2]. Our study sheds light on the understanding of TYLCV–whitefly interactions and provides insights into how a plant virus may evolve to infect and replicate in an insect vector

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Conclusion