Plant microRNAs in larval food regulate honeybee caste development

Zhu, Kegan; Liu, Minghui; Fu, Zheng; Zhou, Zhen; Kong, Yan; Liang, Hongwei; Lin, Zheguang; Luo, Jun; Zheng, Huoqing; Wan, Ping; Zhang, Junfeng; Zen, Ke; Chen, Jiong; Hu, Fuliang; Zhang, Chenyu; Ren, Jie; Chen, Xi

doi:10.1371/journal.pgen.1006946

Cited by 138 publications

(132 citation statements)

References 58 publications

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“…The present knowledge on plant EVs is consistent with the idea of an EV-mediated effector shuttle in ckRNAi [1,22,[48][49][50][51][52][53][54][55]. Here, we tested the possibility that HIGS also involves vesicle transport of dsRNA-derived sRNAs.…”

Section: Exosome-like Vesicles From Leaf Extracts Of Cyp3rna-expressisupporting

confidence: 70%

Host-induced gene silencing involves Arabidopsis ESCRT-III pathway for the transfer of dsRNA-derived siRNA

Schlemmer

Weipert

Barth

et al. 2020

Preprint

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Small (s)RNA molecules are crucial factors in the communication between hosts and their interacting pathogens, where they function as effectors that can modulate both host defense and microbial virulence/pathogenicity through a mechanism termed cross-kingdom RNA interference (ckRNAi). Consistent with this recent knowledge, sRNAs and their doublestranded (ds)RNA precursors have been adopted to control diseases in crop plants through transgenic expression (host-induced gene silencing, HIGS) or exogenous application (sprayinduced gene silencing, SIGS). While these strategies proved to be effective, the mechanism of RNA transfer at the plant -pathogen interface is widely unresolved. Here we show that extracellular vesicles (EVs) purified from Arabidopsis (Arabidopsis thaliana) leaf extracts and apoplastic fluids contain transgene-derived sRNAs. EVs from plants expressing CYP3RNA, a 791 nt long dsRNA, which was originally designed to target the three CYP51 genes of the fungal pathogen Fusarium graminearum, contain CYP3RNA-derived small interfering (si)RNAs as shown by RNA sequencing (RNA-seq) analysis. Notably, the EVs cargo retained the same CYP3RNA-derived siRNA profile as the respective leaf extracts, suggesting that there was no selective uptake of specific artificial sRNAs into EVs. In addition, mutants of the ESCRT-III complex were impaired in HIGS further indicating that endosomal vesicle trafficking supports transfer of transgene-derived siRNAs between donor host cells and recipient fungal cells.Further supporting the relevance of EV-mediated transport of sRNA, we demonstrate that HIGS plants, expressing a 100 nt dsRNA-target-sequence identified via EV-sRNA-seq of CYP3RNA Arabidopsis, confers strong resistance to F. graminearum. Together, these findings support the view that EVs are key mediators in the transport of HIGS-related sRNAs to reduce the virulence of interacting fungal pathogens during host-pathogen interaction.(MVBs) fuse with the PM [33][34][35][36][37]. In mammals, exosomes mediate intercellular communication by shuttling proteins, lipids and RNAs, where RNA molecules remain functional after delivery and can elicit effects in the recipient cell [38][39][40].Based on this knowledge, we speculated that HIGS-and SIGS-related RNAs also are loaded into plant vesicles and transferred by EVs that cross the plant-fungus interface. It was reasoned already more than 50 years ago that a fusion of plant MVBs with the PM may result in the release of small vesicles into the extracellular space [41]. Consistent with this early observation, biogenesis of immune-related MVBs [29,30] and the release of their cargo via EVs also is inherent to the plant secretory pathway [27]. Transmission electron microscopy (TEM) revealed proliferation of MVBs next to plant cell wall papillae in response to infection with powdery mildew fungus and the release of para-mural vesicles. The authors proposed that released vesicles might be similar to exosomes in animal cell thus anticipating that exosomes exist in plants [29,30]. Immun...

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Section: Exosome-like Vesicles From Leaf Extracts Of Cyp3rna-expressisupporting

confidence: 70%

Host-induced gene silencing involves Arabidopsis ESCRT-III pathway for the transfer of dsRNA-derived siRNA

Schlemmer

Weipert

Barth

et al. 2020

Preprint

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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%

“…These findings suggest a naturally occurring transmissible RNA pathway in honey bees. In line with this hypothesis, it has been reported that both worker and royal jellies contain small honey bee RNA populations, demonstrating endogenous bee RNA secretion into the larval diet [17,30]. To further explore the RNA repertoire in the jellies, including the natural occurrence of exogenous and pathogen-related RNA, we adapted a small RNA-seq protocol to sequence fulllength RNA up to 200nt (see materials and methods).…”

Section: Naturally Occurring Rna In Worker and Royal Jelliesmentioning

confidence: 90%

“…Reciprocally, arabidopsis plants secrete and transfer vesicles-containing small RNAs that could suppress virulence fungal genes [16]. Furthermore, ingestion of pollen-derived plant miRNA induces worker bee sterility in a sequence specific manner [17]. Interestingly, while the aforementioned examples provide evidence that some organisms acquire, and are affected by foreign regulatory RNA, it is still puzzling why would they allow it?…”

Section: Introductionmentioning

confidence: 99%

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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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“…RNA exchange even occurs between the different domains of life: the bacterium Salmonella uses the host Argonaute to produce miRNA-like RNA fragments that increase its survival [16] , and mammalian miRNAs present in the gut can be internalized into bacteria and affect their growth thereby shaping the microbiota [17] . Although there has been more focus in the literature on RNA released from pathogens, RNAs are probably being exchanged between all sorts of other interacting species [17][18][19][20] .…”

Section: Introductionmentioning

confidence: 99%

Disentangling sRNA-Seq data to study RNA communication between species

Bermúdez-Barrientos¹,

Ramírez-Sánchez²,

Chow

et al. 2019

Preprint

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Many organisms exchange small RNAs during their interactions, and these RNAs can target or bolster defense strategies in host-pathogen systems. Current sRNA-Seq technology can determine the small RNAs present in any symbiotic system, but there are very few bioinformatic tools available to interpret the results. We show that one of the biggest challenges comes from sequences that map equally well to the genomes of both interacting organisms. This arises due to the small size of the sRNA compared to large genomes, and because many of the produced sRNAs come from genomic regions that encode highly conserved miRNAs, rRNAs or tRNAs. Here we present strategies to disentangle sRNA-Seq data from samples of communicating organisms, developed using diverse plant and animal species that are known to exchange RNA with their parasites. We show that sequence assembly, both de novo and genome-guided, can be used for sRNA-Seq data, greatly reducing the ambiguity of mapping reads. Even confidently mapped sequences can be misleading, so we further demonstrate the use of differential expression strategies to determine the true parasitic sRNAs within host cells. Finally, we validate our methods on new experiments designed to probe the nature of the extracellular vesicle sRNAs from the parasitic nematode H. bakeri that get into mouse epithelial cells.

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Plant microRNAs in larval food regulate honeybee caste development

Cited by 138 publications

References 58 publications

Host-induced gene silencing involves Arabidopsis ESCRT-III pathway for the transfer of dsRNA-derived siRNA

Host-induced gene silencing involves Arabidopsis ESCRT-III pathway for the transfer of dsRNA-derived siRNA

A transmissible RNA pathway in honey bees

Disentangling sRNA-Seq data to study RNA communication between species

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