A Transmissible RNA Pathway in Honey Bees

Eyal Maori; Yael Garbian; Vered Kunik; Rita Mozes-Koch; Osnat Malka; Haim Kalev; Niv Sabath; Ilan Sela; Sharoni Shafir

doi:10.1016/j.celrep.2019.04.073

A Transmissible RNA Pathway in Honey Bees

Eyal Maori^*, Yael Garbian, Vered Kunik, Rita Mozes-Koch, Osnat Malka, Haim Kalev, Niv Sabath, Ilan Sela, Sharoni Shafir

^*Corresponding author for this work

Department of Entomology

Research output: Contribution to journal › Article › peer-review

32 Scopus citations

Abstract

Systemic RNAi, initiated by double-stranded RNA (dsRNA) ingestion, has been reported in diverse invertebrates, including honey bees, demonstrating environmental RNA uptake that undermines homologous gene expression. However, the question why any organism would take up RNA from the environment has remained largely unanswered. Here, we report on horizontal RNA flow among honey bees mediated by secretion and ingestion of worker and royal jelly diets. We demonstrate that transmission of jelly-secreted dsRNA to larvae is biologically active and triggers gene knockdown that lasts into adulthood. Worker and royal jellies harbor differential naturally occurring RNA populations. Jelly RNAs corresponded to honey bee protein-coding genes, transposable elements, and non-coding RNA, as well as bacteria, fungi, and viruses. These results reveal an inherent property of honey bees to share RNA among individuals and generations. Our findings suggest a transmissible RNA pathway, playing a role in social immunity and signaling between members of the hive. RNA mobility among cells has been documented in plants and animals. Maori et al. show that RNA spreads further in honey bees and is horizontally transferred between individuals and across generations. Their findings demonstrate a transmissible RNA pathway with potential roles in social immunity and epigenetic communication between honey bees.

Original language	American English
Pages (from-to)	1949-1959.e6
Journal	Cell Reports
Volume	27
Issue number	7
DOIs	https://doi.org/10.1016/j.celrep.2019.04.073
State	Published - 14 May 2019

Bibliographical note

Funding Information:
Professor Ilan Sela, who died aged 81, was Professor of Virology and Molecular Biology at the Hebrew University of Jerusalem and was regarded as one of the pioneer virologists in Israel. Ilan was a creative mind and a passionate scientist. He found joy in understanding fundamental principles in biology and reveled in their translation into real world solutions. For more than five decades, he nourished generations of students with curiosity and admiration toward science. Ilan is greatly missed. The authors thank Dr. Ed Farnell and Dr Emily Clemente from Cambridge Genomic Services for their contribution in the RNA-seq protocol development. We thank Mr. John Rayner (Springwell Apiaries, UK) for his support on bee and jelly samples. We are grateful to Prof. Eric Miska, Prof. Jonathan Heeney, and their groups, as well as to Professor Sir Peter Lachmann, Mr. David Seilly, Dr. Laurence Tiley, and Dr. Shahar Avin (Cambridge University) for inspiring discussions and advice. This work was supported by internal B. Triwaks Bee Research Center funds ( HUJI no. 0356043 ), the Orion Foundation (HUJI no. 0368598 ), and Israel Science Foundation (grant no. 1456/10 ) to S.S. Research was also supported by Marie Curie Intra-European Fellowship For Career Development ( PIEF-GA-2010-274406 ), Leo Baeck Scholarship, and Herchel Smith Postdoctoral Fellowship ( XXACC_AFGLTRB2 ) to E.M.

Publisher Copyright:
© 2019 The Authors

Keywords

Honey bees
RNA transmission
RNAi
RNP
eRNA
environmental RNA
extracellular RNA
royal jelly
transmissible RNA
viruses

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10.1016/j.celrep.2019.04.073

Cite this

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title = "A Transmissible RNA Pathway in Honey Bees",

abstract = "Systemic RNAi, initiated by double-stranded RNA (dsRNA) ingestion, has been reported in diverse invertebrates, including honey bees, demonstrating environmental RNA uptake that undermines homologous gene expression. However, the question why any organism would take up RNA from the environment has remained largely unanswered. Here, we report on horizontal RNA flow among honey bees mediated by secretion and ingestion of worker and royal jelly diets. We demonstrate that transmission of jelly-secreted dsRNA to larvae is biologically active and triggers gene knockdown that lasts into adulthood. Worker and royal jellies harbor differential naturally occurring RNA populations. Jelly RNAs corresponded to honey bee protein-coding genes, transposable elements, and non-coding RNA, as well as bacteria, fungi, and viruses. These results reveal an inherent property of honey bees to share RNA among individuals and generations. Our findings suggest a transmissible RNA pathway, playing a role in social immunity and signaling between members of the hive. RNA mobility among cells has been documented in plants and animals. Maori et al. show that RNA spreads further in honey bees and is horizontally transferred between individuals and across generations. Their findings demonstrate a transmissible RNA pathway with potential roles in social immunity and epigenetic communication between honey bees.",

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note = "Funding Information: Professor Ilan Sela, who died aged 81, was Professor of Virology and Molecular Biology at the Hebrew University of Jerusalem and was regarded as one of the pioneer virologists in Israel. Ilan was a creative mind and a passionate scientist. He found joy in understanding fundamental principles in biology and reveled in their translation into real world solutions. For more than five decades, he nourished generations of students with curiosity and admiration toward science. Ilan is greatly missed. The authors thank Dr. Ed Farnell and Dr Emily Clemente from Cambridge Genomic Services for their contribution in the RNA-seq protocol development. We thank Mr. John Rayner (Springwell Apiaries, UK) for his support on bee and jelly samples. We are grateful to Prof. Eric Miska, Prof. Jonathan Heeney, and their groups, as well as to Professor Sir Peter Lachmann, Mr. David Seilly, Dr. Laurence Tiley, and Dr. Shahar Avin (Cambridge University) for inspiring discussions and advice. This work was supported by internal B. Triwaks Bee Research Center funds ( HUJI no. 0356043 ), the Orion Foundation (HUJI no. 0368598 ), and Israel Science Foundation (grant no. 1456/10 ) to S.S. Research was also supported by Marie Curie Intra-European Fellowship For Career Development ( PIEF-GA-2010-274406 ), Leo Baeck Scholarship, and Herchel Smith Postdoctoral Fellowship ( XXACC_AFGLTRB2 ) to E.M. Publisher Copyright: {\textcopyright} 2019 The Authors",

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AU - Kalev, Haim

AU - Sabath, Niv

AU - Sela, Ilan

AU - Shafir, Sharoni

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KW - RNAi

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KW - extracellular RNA

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KW - viruses

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A Transmissible RNA Pathway in Honey Bees

Abstract

Bibliographical note

Keywords

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