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A Transmissible RNA Pathway in Honey Bees
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 re...
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Published in: | Cell reports (Cambridge) 2019-05, Vol.27 (7), p.1949-1959.e6 |
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container_end_page | 1959.e6 |
container_issue | 7 |
container_start_page | 1949 |
container_title | Cell reports (Cambridge) |
container_volume | 27 |
creator | Maori, Eyal Garbian, Yael Kunik, Vered Mozes-Koch, Rita Malka, Osnat Kalev, Haim Sabath, Niv Sela, Ilan Shafir, Sharoni |
description | 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.
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•Ingested dsRNA spreads via hemolymph and is secreted in worker and royal jellies•Functional dsRNA flows horizontally among honey bees by jelly consumption•Worker and royal jellies harbor differential natural ssRNA and dsRNA populations•Diverse pathogenic RNA fragments naturally occur in worker and royal jellies
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. |
doi_str_mv | 10.1016/j.celrep.2019.04.073 |
format | article |
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[Display omitted]
•Ingested dsRNA spreads via hemolymph and is secreted in worker and royal jellies•Functional dsRNA flows horizontally among honey bees by jelly consumption•Worker and royal jellies harbor differential natural ssRNA and dsRNA populations•Diverse pathogenic RNA fragments naturally occur in worker and royal jellies
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.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2019.04.073</identifier><identifier>PMID: 31056439</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>environmental RNA ; eRNA ; extracellular RNA ; Honey bees ; RNA transmission ; RNAi ; RNP ; royal jelly ; transmissible RNA ; viruses</subject><ispartof>Cell reports (Cambridge), 2019-05, Vol.27 (7), p.1949-1959.e6</ispartof><rights>2019 The Authors</rights><rights>Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-406261e34e6467b244eead5035182d2c32191b07c33a8f312be80829a98223b3</citedby><cites>FETCH-LOGICAL-c474t-406261e34e6467b244eead5035182d2c32191b07c33a8f312be80829a98223b3</cites><orcidid>0000-0002-9541-9554</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31056439$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Maori, Eyal</creatorcontrib><creatorcontrib>Garbian, Yael</creatorcontrib><creatorcontrib>Kunik, Vered</creatorcontrib><creatorcontrib>Mozes-Koch, Rita</creatorcontrib><creatorcontrib>Malka, Osnat</creatorcontrib><creatorcontrib>Kalev, Haim</creatorcontrib><creatorcontrib>Sabath, Niv</creatorcontrib><creatorcontrib>Sela, Ilan</creatorcontrib><creatorcontrib>Shafir, Sharoni</creatorcontrib><title>A Transmissible RNA Pathway in Honey Bees</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>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.
[Display omitted]
•Ingested dsRNA spreads via hemolymph and is secreted in worker and royal jellies•Functional dsRNA flows horizontally among honey bees by jelly consumption•Worker and royal jellies harbor differential natural ssRNA and dsRNA populations•Diverse pathogenic RNA fragments naturally occur in worker and royal jellies
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.</description><subject>environmental RNA</subject><subject>eRNA</subject><subject>extracellular RNA</subject><subject>Honey bees</subject><subject>RNA transmission</subject><subject>RNAi</subject><subject>RNP</subject><subject>royal jelly</subject><subject>transmissible RNA</subject><subject>viruses</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9kE1rG0EMhofS0AQn_6CUPaYHb6QZeT8uATe0TSC0pfg-zIfcjFnvOjPrFP_7jrtp6Cm6SIhX74seId4jlAhYXW1Kx13kXSkB2xKohFq9EWdSIs5RUv32v_lUXKS0gVwVILb0TpwqhEVFqj0TH5fFKpo-bUNKwXZc_Py2LH6Y8eG3ORShL26Hng_FJ-Z0Lk7Wpkt88dxnYvXl8-rmdn7__evdzfJ-7qimcU5QyQpZEVdU1VYSMRu_ALXARnrplMQWLdROKdOsFUrLDTSyNW0jpbJqJu4mWz-Yjd7FsDXxoAcT9N_FEH9pE8fgOtYOJThvyRA11DRovLcL69bWeQaSR6_LyWsXh8c9p1HnNzO4zvQ87JPOgRJURbnPBE1SF4eUIq9fohH0Ebne6Am5PiLXQDojz2cfnhP2dsv-5egf4Cy4ngSckT0Fjjq5wL1jHyK7MT8VXk_4A1syj_k</recordid><startdate>20190514</startdate><enddate>20190514</enddate><creator>Maori, Eyal</creator><creator>Garbian, Yael</creator><creator>Kunik, Vered</creator><creator>Mozes-Koch, Rita</creator><creator>Malka, Osnat</creator><creator>Kalev, Haim</creator><creator>Sabath, Niv</creator><creator>Sela, Ilan</creator><creator>Shafir, Sharoni</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9541-9554</orcidid></search><sort><creationdate>20190514</creationdate><title>A Transmissible RNA Pathway in Honey Bees</title><author>Maori, Eyal ; Garbian, Yael ; Kunik, Vered ; Mozes-Koch, Rita ; Malka, Osnat ; Kalev, Haim ; Sabath, Niv ; Sela, Ilan ; Shafir, Sharoni</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-406261e34e6467b244eead5035182d2c32191b07c33a8f312be80829a98223b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>environmental RNA</topic><topic>eRNA</topic><topic>extracellular RNA</topic><topic>Honey bees</topic><topic>RNA transmission</topic><topic>RNAi</topic><topic>RNP</topic><topic>royal jelly</topic><topic>transmissible RNA</topic><topic>viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Maori, Eyal</creatorcontrib><creatorcontrib>Garbian, Yael</creatorcontrib><creatorcontrib>Kunik, Vered</creatorcontrib><creatorcontrib>Mozes-Koch, Rita</creatorcontrib><creatorcontrib>Malka, Osnat</creatorcontrib><creatorcontrib>Kalev, Haim</creatorcontrib><creatorcontrib>Sabath, Niv</creatorcontrib><creatorcontrib>Sela, Ilan</creatorcontrib><creatorcontrib>Shafir, Sharoni</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maori, Eyal</au><au>Garbian, Yael</au><au>Kunik, Vered</au><au>Mozes-Koch, Rita</au><au>Malka, Osnat</au><au>Kalev, Haim</au><au>Sabath, Niv</au><au>Sela, Ilan</au><au>Shafir, Sharoni</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Transmissible RNA Pathway in Honey Bees</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2019-05-14</date><risdate>2019</risdate><volume>27</volume><issue>7</issue><spage>1949</spage><epage>1959.e6</epage><pages>1949-1959.e6</pages><issn>2211-1247</issn><eissn>2211-1247</eissn><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.
[Display omitted]
•Ingested dsRNA spreads via hemolymph and is secreted in worker and royal jellies•Functional dsRNA flows horizontally among honey bees by jelly consumption•Worker and royal jellies harbor differential natural ssRNA and dsRNA populations•Diverse pathogenic RNA fragments naturally occur in worker and royal jellies
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.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31056439</pmid><doi>10.1016/j.celrep.2019.04.073</doi><orcidid>https://orcid.org/0000-0002-9541-9554</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | environmental RNA eRNA extracellular RNA Honey bees RNA transmission RNAi RNP royal jelly transmissible RNA viruses |
title | A Transmissible RNA Pathway in Honey Bees |
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