Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera

Esmaeil Amiri; Jacob J Herman; Micheline K Strand; David R Tarpy; Olav Rueppell

doi:10.1016/j.meegid.2020.104558

Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera

Infect Genet Evol. 2020 Nov:85:104558. doi: 10.1016/j.meegid.2020.104558. Epub 2020 Sep 16.

Authors

Esmaeil Amiri¹, Jacob J Herman², Micheline K Strand³, David R Tarpy⁴, Olav Rueppell⁵

Affiliations

¹ Department of Biology, University of North Carolina at Greensboro, Greensboro, NC 27402, USA; Department of Entomology & Plant Pathology, North Carolina State University, Raleigh, NC 27695, USA. Electronic address: e.amiri79@gmail.com.
² Department of Biology, University of North Carolina at Greensboro, Greensboro, NC 27402, USA.
³ Life Sciences Division, U.S. Army Research Office, CCDC-ARL, Research Triangle Park, Durham, NC 27709, USA.
⁴ Department of Entomology & Plant Pathology, North Carolina State University, Raleigh, NC 27695, USA.
⁵ Department of Biology, University of North Carolina at Greensboro, Greensboro, NC 27402, USA; Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada.

PMID: 32947033
DOI: 10.1016/j.meegid.2020.104558

Abstract

Trans-generational disease effects include vertical pathogen transmission but also immune priming to enhance offspring immunity. Accordingly, the survival consequences of maternal virus infection can vary and its molecular consequences during early development are poorly understood. The honey bee queen is long-lived and represents the central hub for vertical virus transmission as the sole reproductive individual in her colony. Even though virus symptoms in queens are mild, viral infection may have severe consequences for the offspring. Thus, transcriptome patterns during early developmental are predicted to respond to maternal virus infection. To test this hypothesis, gene expression patterns were compared among pooled honey bee eggs laid by queens that were either infected with Deformed wing virus (DWV¹), Sacbrood virus (SBV²), both viruses (DWV and SBV), or no virus. Whole transcriptome analyses revealed significant expression differences of a few genes, some of which have hitherto no known function. Despite the paucity of single gene effects, functional enrichment analyses revealed numerous biological processes in the embryos to be affected by virus infection. Effects on several regulatory pathways were consistent with maternal responses to virus infection and correlated with responses to DWV and SBV in honey bee larvae and pupae. Overall, effects on egg transcriptome patterns were specific to each virus and the results of dual-infection samples suggested synergistic effects of DWV and SBV. We interpret our results as consequences of maternal infections. Thus, this first study to document and characterize virus-associated changes in the transcriptome of honey bee eggs represents an important contribution to understanding trans-generational virus effects, although more in-depth studies are needed to understand the detailed mechanisms of how viruses affect honey bee embryos.

Keywords: Deformed wing virus; Egg; Honey bee queen; Immune priming; Sacbrood virus; Trans-generational disease.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animal Diseases / genetics*
Animal Diseases / virology*
Animals
Bees / virology*
Female
Gene Expression Profiling
RNA Viruses
Transcriptome*
Virus Diseases / veterinary*

Supplementary concepts

Deformed wing virus