IAPV, a bee‐affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion

Maori, Eyal; Paldi, Nitzan; Shafir, Sharoni; Kalev, Haim; Tsur, Erez; Glick, Eitan; Sela, Ilan

doi:10.1111/j.1365-2583.2009.00847.x

Cited by 219 publications

(224 citation statements)

References 17 publications

(28 reference statements)

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“…Aside from the above mortality and sub-lethal effects, the symptoms associated with IAPV have not been well characterized and thus hinder our ability to observe the progression of IAPV infection in these important pollinators, especially when considering that virus-induced paralysis symptoms are normally the signal of overt infection and death. Besides, the initial observation of IAPV symptoms are from honeybees; symptom analysis in bumblebees would enhance our knowledge of this virus (de Miranda et al, 2010;DeGrandi-Hoffman & Chen, 2015;Maori et al, 2007Maori et al, , 2009Piot et al, 2015). Therefore, in this study, we report progressive viral symptoms in workers of B. terrestris, which is one of the most numerous bumblebee species in Europe (Velthuis & van Doorn, 2006).…”

Section: Introductionmentioning

confidence: 95%

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Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Wang

Meeus

Smagghe

2016

Journal of General Virology

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Although it is known that Israeli acute paralysis virus (IAPV) can cause bee mortality, the symptoms of paralysis and the distribution of the virus in different body tissues and their potential to respond with an increase of the siRNA antiviral immune system have not been studied. In this project we worked with Bombus terrestris, which is one of the most numerous bumblebee species in Europe and an important pollinator for wild flowers and many crops in agriculture. Besides the classic symptoms of paralysis and trembling prior to death, we report a new IAPVrelated symptom, crippled/immobilized forelegs. Reverse-transcriptase quantitative PCR showed that IAPV accumulates in different body tissues (midgut, fat body, brain and ovary). The highest levels of IAPV were observed in the fat body. With fluorescence in situ hybridization (FISH) we detected IAPV in the Kenyon cells of mushroom bodies and neuropils from both antennal and optic lobes of the brain in IAPV-infected workers. Finally, we observed an induction of Dicer-2, a core gene of the RNAi antiviral immune response, in the IAPV-infected tissues of B. terrestris workers. According to our results, tissue tropism and the induction strength of Dicer-2 could not be correlated with virus-related paralysis symptoms. INTRODUCTIONHoneybees and bumblebees are the two most important bee species used in modern apiculture and agriculture. They host many viruses. When looking at the honeybee, there have been around 23 viruses reported and many of these viruses only persist as covert and asymptomatic infections which show no detectable impact at both the individual and colony level (McMenamin & Genersch, 2015). However, under certain conditions, for example the presence of the ectoparasitic honeybee mite Varroa destructor, the covert infections of some viruses turn into overt ones with observable symptoms (Martin et al., 2012;McMahon et al., 2015;Singh et al., 2010). The symptoms of overt infections vary from virus to virus, including deformed wings, discoloration, hair losses, bloated abdomen, paralysis, decreased locomotion, impaired cognition and both brood and adult mortality (Lanzi et al., 2006;McMenamin & Genersch, 2015;Singh et al., 2010). Some symptoms can be easily recognized by the behaviour and appearance of the infected bees, while others can only be confirmed through meticulous and continuous observations or by molecular techniques.In bumblebees (Bombus spp.) a subset of honeybee-infecting viruses has been reported, such as deformed wing virus (DWV), Israeli acute paralysis virus (IAPV), acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), slow bee paralysis virus (SBPV), sacbrood virus (SBV), black queen cell virus (BQCV) and Lake Sinai virus (LSV) (Genersch et al., 2006;Levitt et al., 2013;Parmentier et al., 2016;Peng et al., 2011). However, only DWV, KBV and IAPV have been reported to cause clinical symptoms (Genersch et al., 2006;Meeus et al., 2014). DWV caused crippled wings in bumblebee (Bombus terrestris and Bombus pascuorum) workers even without ...

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Section: Introductionmentioning

confidence: 95%

“…The nomenclature of this virus is largely based on its symptoms that are similar to ABPV. Both viruses can induce abnormal body trembling (Galbraith et al, 2015;Li et al, 2013;Maori et al, 2009). In bumblebees, injection of a low dose of IAPV particles into healthy workers could induce rapid mortality (Niu et al, 2014a).…”

Section: Introductionmentioning

confidence: 99%

Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Wang

Meeus

Smagghe

2016

Journal of General Virology

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“…Different episodes of mortality and reductions in honey production associated with viral infections have been reported worldwide (Chen et al, 2005;Chen and Siede, 2007;Bacandritsos et al, 2010;Gumusova et al, 2010;Genersch and Aubert, 2010;Ai et al, 2012). In effect, there is increasing concern about the effect of viral infections on honey bee populations, largely due to the potential relation between viral diseases and honey bee mortality (Cox Foster et al, 2007;Maori et al, 2009;Hunter et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens

Rodríguez¹,

Vargas²,

Antúnez

et al. 2014

Chilean J. Agric. Res.

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Different episodes of mortalities of honey bee (Apis mellifera L.) colonies have been associated with the presence of honey bee pathogens. Since the Biobío Region has among the highest number of apiaries in Chile, the aim of the present study was to identify viruses in the Region affecting honey bees, evaluate their relation to other pathogens, and conduct a phylogenetic analysis. Pupae and adult bees were collected from 60 apiaries of Apis mellifera L. in the Biobío Region over 2 yr. RNA viruses were detected by reverse transcription PCR (RT-PCR), and Acarapis woodi, Nosema spp., and Varroa destructor via PCR. Three viruses were detected: Acute bee paralysis virus (ABPV), Black queen cell virus (BQCV) and Deformed wing virus (DWV) in 2%, 10%, and 42% of the apiaries, respectively. No statistical correlation was observed between the presence of the different viruses, V. destructor, A. woodi, and the two Nosema species, and the bee development stages. One year after the first sampling, DWV and BQCV were detected mainly in foraging adult bee samples. Three percent of the apiaries were infected with N. apis and 18% with N. ceranae, 5% were positive for V. destructor, while A. woodi was not detected. PCR products were sequenced and compared to the Genbank database. Chilean sequences of ABPV, BQCV, and DWV showed high percentages of similarity to other isolates in South America.

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“…In agreement, oral administration of dsRNA appears to be effective at regulation of gene expression in honey bees. [69][70][71][72][73][74][75][76] In addition, high dose injection of dsRNAs into the hemocoel has been used for delivery and inhibition of target genes in multiple tissues in this species [77][78][79][80][81][82][83][84][85][86] independent of the site of injection, demonstrating that these molecules can be efficiently taken up by disparate tissues once in the open circulatory system. Our results, in conjunction with the previous studies using dsRNA in other insect species, suggest that uptake of longer dsRNAs may be more efficient than shorter miRNAs.…”

Section: Discussionmentioning

confidence: 99%

Negligible uptake and transfer of diet-derived pollen microRNAs in adult honey bees

et al. 2015

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The putative transfer and gene regulatory activities of diet-derived miRNAs in ingesting animals are still debated. Importantly, no study to date has fully examined the role of dietary uptake of miRNA in the honey bee, a critical pollinator in both agricultural and natural ecosystems. After controlled pollen feeding experiments in adult honey bees, we observed that midguts demonstrated robust increases in plant miRNAs after pollen ingestion. However, we found no evidence of biologically relevant delivery of these molecules to proximal or distal tissues of recipient honey bees. Our results, therefore, support the premise that pollen miRNAs ingested as part of a typical diet are not robustly transferred across barrier epithelia of adult honey bees under normal conditions. Key future questions include whether other small RNA species in honey bee diets behave similarly and whether more specialized and specific delivery mechanisms exist for more efficient transport, particularly in the context of stressed barrier epithelia.

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IAPV, a bee‐affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion

Cited by 219 publications

References 17 publications

Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens

Negligible uptake and transfer of diet-derived pollen microRNAs in adult honey bees

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