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

Masood, Maryam; Everett, Claire P.; Chan, Stephen Y.; Snow, Jonathan W.

doi:10.1080/15476286.2015.1128063

Cited by 40 publications

(37 citation statements)

References 93 publications

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“…Unfortunately, even in Drosophila mechanisms of JH uptake by tissues are still unclear (Rodríguez-Vázquez et al, 2015; Engelmann and Mala, 2000; Suzuki et al, 2011; Parra-Peralbo and Culi, 2011). Extracellular miRNAs are secreted and transported through a variety of pathways, but the functional relevance of such molecules is still controversial (Sarkies and Miska, 2013; Turchinovich et al, 2016; Masood et al, 2016; Søvik et al, 2015; Rayner and Hennessy, 2013). …”

Section: Discussionmentioning

confidence: 99%

Oral transfer of chemical cues, growth proteins and hormones in social insects

LeBoeuf

Waridel

Brent

et al. 2016

eLife

112

123

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Social insects frequently engage in oral fluid exchange – trophallaxis – between adults, and between adults and larvae. Although trophallaxis is widely considered a food-sharing mechanism, we hypothesized that endogenous components of this fluid might underlie a novel means of chemical communication between colony members. Through protein and small-molecule mass spectrometry and RNA sequencing, we found that trophallactic fluid in the ant Camponotus floridanus contains a set of specific digestion- and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. When C. floridanus workers’ food was supplemented with this hormone, the larvae they reared via trophallaxis were twice as likely to complete metamorphosis and became larger workers. Comparison of trophallactic fluid proteins across social insect species revealed that many are regulators of growth, development and behavioral maturation. These results suggest that trophallaxis plays previously unsuspected roles in communication and enables communal control of colony phenotypes.DOI: http://dx.doi.org/10.7554/eLife.20375.001

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Section: Discussionmentioning

confidence: 99%

Oral transfer of chemical cues, growth proteins and hormones in social insects

LeBoeuf

Waridel

Brent

et al. 2016

eLife

112

123

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“…However, the ability of bees to efficiently take up dietary small RNAs (e.g. miRNAs, siRNAs) is currently debatable [17,30,34,35]. While exchange of dietary RNA among adult bees can reasonably occur via trophallaxis [36], in our experiments, secretion of jelly that contained dsRNA-GFP required systemic distribution of the environmentally consumed dsRNA within the nurse bee.…”

Section: Discussionmentioning

confidence: 75%

A transmissible RNA pathway in honey bees

Maori¹,

Garbian

Kunik³

et al. 2018

Preprint

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SIGNIFICANCEHoney bees are eusocial insects, living in a colony that is often described as a superorganism. RNA mobility among cells of an organism has been documented in plants and animals. Here we show that RNA spreads further in honey bees, and is horizontally transferred between individuals and across generations. We found that honey bees share biologically active RNA through secretion and ingestion of worker and royal jellies. Such RNA initiated RNA interference, which is a known defense mechanism against viral infection. Furthermore, we characterized diverse RNA profiles of worker and royal jelly, including fragmented viral RNA. Our findings demonstrate a transmissible RNA pathway with potential roles in social immunity and epigenetic signaling among members of the hive. ABSTRACTOne of the characteristics of RNA interference (RNAi) is systemic spread of the silencing signal among cells and tissues throughout the organism. 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 show that ingested dsRNA spreads through the bee's hemolymph associated with a protein complex. The systemic dsRNA is secreted with the jelly and delivered to larvae via ingestion. Furthermore, we demonstrate that transmission of jelly-secreted dsRNA to larvae is biologically active and triggers gene knockdown that lasts into adulthood. Finally, RNA extracted from worker and royal jellies harbor differential naturally occurring RNA populations. Some of these RNAs corresponded to honey bee protein coding genes, transposable elements, non-coding RNA and exogenous viruses. These results reveal an inherent property of honey bees to share RNA among individuals and generations. Thus, our findings suggest a transmissible RNA pathway, playing a role in social immunity and epigenetic dynamics among honey bees and potentially other closely interacting organisms.

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“…37 Finally, our own group found no evidence of biologically relevant delivery of a miRNA species highly expressed in dietary pollen to proximal or distal tissues of recipient honey bees. 30,38 Taken together, these data suggest that natural sRNA uptake is variable and possibly dependent on the sRNA biotype and invertebrate species examined. A more complete understanding of the natural uptake of diet-derived sRNA by invertebrate species could have significant implications for our understanding of ecological relationships and our use of RNAi technology in an agricultural setting.…”

Section: Introductionmentioning

confidence: 83%

Uptake and impact of natural diet-derived small RNA in invertebrates: Implications for ecology and agriculture

Chan

Snow

2016

RNA Biology

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The putative transfer and gene regulatory activities of diet-derived small RNAs (sRNAs) in ingesting animals are still debated. The existence of natural uptake of diet-derived sRNA by invertebrate species could have significant implication for our understanding of ecological relationships and could synergize with efforts to use RNA interference (RNAi) technology in agriculture. Here, we synthesize information gathered from studies in invertebrates using natural or artificial dietary delivery of sRNA and from studies of sRNA in vertebrate animals and plants to review our current understanding of uptake and impact of natural dietderived sRNA on invertebrates. Our understanding has been influenced and sometimes confounded by the diversity of invertebrates and ingested plants studied, our limited insights into how gene expression may be modulated by dietary sRNAs at the mechanistic level, and the paucity of studies focusing directly on natural uptake of sRNA. As such, we suggest 2 strategies to investigate this phenomenon more comprehensively and thus facilitate the realization of its potentially broad impact on ecology and agriculture in the future.

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

Cited by 40 publications

References 93 publications

Oral transfer of chemical cues, growth proteins and hormones in social insects

Oral transfer of chemical cues, growth proteins and hormones in social insects

A transmissible RNA pathway in honey bees

Uptake and impact of natural diet-derived small RNA in invertebrates: Implications for ecology and agriculture

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