Abstract

Bemisia tabaci (Gennadius) is one of the economically most damaging insects to crops in tropical and subtropical regions. Severe damage is caused by feeding and more seriously by transmitting viruses. Those of the genus begomovirus (Geminiviridae) cause the most significant crop diseases and are transmitted by B. tabaci in a persistent circulative mode, a process which is largely unknown. To analyze the translocation and to identify critical determinants for transmission, two populations of B. tabaci MEAM1 were compared for transmitting Watermelon chlorotic stunt virus (WmCSV) and Tomato yellow leaf curl virus (TYLCV). Insect populations were chosen because of their high and respectively low virus transmission efficiency to compare uptake and translocation of virus through insects. Both populations harbored Rickettsia, Hamiltonella and Wolbachia in comparable ratios indicating that endosymbionts might not contribute to the different transmission rates. Quantification by qPCR revealed that WmCSV uptake and virus concentrations in midguts and primary salivary glands were generally higher than TYLCV due to higher virus contents of the source plants. Both viruses accumulated higher in insects from the efficiently compared to the poorly transmitting population. In the latter, virus translocation into the hemolymph was delayed and virus passage was impeded with limited numbers of viruses translocated. FISH analysis confirmed these results with similar virus distribution found in excised organs of both populations. No virus accumulation was found in the midgut lumen of the poor transmitter because of a restrained virus translocation. Results suggest that the poorly transmitting population comprised insects that lacked transmission competence. Those were selected to develop a population that lacks virus transmission. Investigations with insects lacking transmission showed that virus concentrations in midguts were reduced and only negligible virus amounts were found at the primary salivary glands indicating for a missing or modified receptor responsible for virus attachment or translocation.

Highlights

  • The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is an agricultural pest in tropical and subtropical regions

  • We have investigated the translocation of circular transmitted begomoviruses, Watermelon chlorotic stunt virus (WmCSV) and Tomato yellow leaf curl virus (TYLCV), in populations of B. tabaci 63 and 95 that were chosen for their differential capabilities to transmit the viruses

  • We found an enhanced transcription of hsp70 in B. tabaci 63 after virus uptake and increased virus transmission after antiHSP70 antibody feeding [37]

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Summary

Introduction

The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is an agricultural pest in tropical and subtropical regions It is a polyphagous phloem-feeder that causes damage in many crops due to direct feeding and vectoring of numerous plant viruses [1,2]. Tomato yellow leaf curl virus (TYLCV) has a monopartite genome [29] while that of Watermelon chlorotic stunt virus (WmCSV) is bipartite with a DNA-A and a DNA-B genomic component [11] Both cause serious crop diseases: WmCSV threatens the production of cucurbit crops like watermelon (Citrullus lanatus), melons (Cucumis melo), and pumpkin (Cucurbita moschata) in North Africa, Yemen, Israel, Jordan and Iran [12]. Symptoms on tomato consist of a more or less pronounced upward curling of PLOS ONE | www.plosone.org leaflets and leaf yellowing which is most prominent on young leaves in the apical parts of the plants

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