Inviting an author to review:
Find an author and click ‘Invite to review selected article’ near their name.
Search for authorsSearch for similar articles
30
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Plant microRNAs in larval food regulate honeybee caste development

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The major environmental determinants of honeybee caste development come from larval nutrients: royal jelly stimulates the differentiation of larvae into queens, whereas beebread leads to worker bee fate. However, these determinants are not fully characterized. Here we report that plant RNAs, particularly miRNAs, which are more enriched in beebread than in royal jelly, delay development and decrease body and ovary size in honeybees, thereby preventing larval differentiation into queens and inducing development into worker bees. Mechanistic studies reveal that amTOR, a stimulatory gene in caste differentiation, is the direct target of miR162a. Interestingly, the same effect also exists in non-social Drosophila. When such plant RNAs and miRNAs are fed to Drosophila larvae, they cause extended developmental times and reductions in body weight and length, ovary size and fecundity. This study identifies an uncharacterized function of plant miRNAs that fine-tunes honeybee caste development, offering hints for understanding cross-kingdom interaction and co-evolution.

          Author summary

          How caste has formed in honeybees is an enduring puzzle. The prevailing view is that royal jelly stimulates the differentiation of larvae into queen. Here, we uncover a new mechanism that plant miRNAs in worker bee’s food postpone larval development, thereby inducing sterile worker bees. Thus, the theories about honeybee caste formation need to be re-examined from a new angle besides the traditional focus on royal jelly and its components. Furthermore, since miRNAs are transmitted between species of different kingdoms and can contribute to the phenotype regulation, this new model of horizontal miRNA transfer may open up a new avenue to further study the molecular mechanisms underlying cross-kingdom interaction and co-evolution.

          Related collections

          Most cited references48

          • Record: found
          • Abstract: found
          • Article: not found

          Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways.

          Botrytis cinerea, the causative agent of gray mold disease, is an aggressive fungal pathogen that infects more than 200 plant species. Here, we show that some B. cinerea small RNAs (Bc-sRNAs) can silence Arabidopsis and tomato genes involved in immunity. These Bc-sRNAs hijack the host RNA interference (RNAi) machinery by binding to Arabidopsis Argonaute 1 (AGO1) and selectively silencing host immunity genes. The Arabidopsis ago1 mutant exhibits reduced susceptibility to B. cinerea, and the B. cinerea dcl1 dcl2 double mutant that can no longer produce these Bc-sRNAs displays reduced pathogenicity on Arabidopsis and tomato. Thus, this fungal pathogen transfers "virulent" sRNA effectors into host plant cells to suppress host immunity and achieve infection, which demonstrates a naturally occurring cross-kingdom RNAi as an advanced virulence mechanism.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol.

            We identify a cytochrome P450 gene (CYP6AE14) from cotton bollworm (Helicoverpa armigera), which permits this herbivore to tolerate otherwise inhibitory concentrations of the cotton metabolite, gossypol. CYP6AE14 is highly expressed in the midgut and its expression correlates with larval growth when gossypol is included in the diet. When larvae are fed plant material expressing double-stranded RNA (dsRNA) specific to CYP6AE14, levels of this transcript in the midgut decrease and larval growth is retarded. Both effects are more dramatic in the presence of gossypol. As a glutathione-S-transferase gene (GST1) is silenced in GST1 dsRNA-expressing plants, feeding insects plant material expressing dsRNA may be a general strategy to trigger RNA interference and could find applications in entomological research and field control of insect pests.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1.

              Double-stranded RNA-mediated gene interference (RNAi) in Caenorhabditis elegans systemically inhibits gene expression throughout the organism. To investigate how gene-specific silencing information is transmitted between cells, we constructed a strain that permits visualization of systemic RNAi. We used this strain to identify systemic RNA interference-deficient (sid) loci required to spread gene-silencing information between tissues but not to initiate or maintain an RNAi response. One of these loci, sid-1, encodes a conserved protein with predicted transmembrane domains. SID-1 is expressed in cells sensitive to RNAi, is localized to the cell periphery, and is required cell-autonomously for systemic RNAi.
                Bookmark

                Author and article information

                Contributors
                Role: InvestigationRole: MethodologyRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: Visualization
                Role: InvestigationRole: Writing – review & editing
                Role: SoftwareRole: Visualization
                Role: Investigation
                Role: Methodology
                Role: InvestigationRole: Methodology
                Role: Investigation
                Role: Methodology
                Role: Investigation
                Role: Supervision
                Role: SupervisionRole: Writing – review & editing
                Role: Resources
                Role: Resources
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                31 August 2017
                August 2017
                : 13
                : 8
                : e1006946
                Affiliations
                [1 ] State Key Laboratory of Pharmaceutical Biotechnology, NJU Advanced Institute for Life Sciences, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Nanjing University, Nanjing, China
                [2 ] College of Animal Science, Zhejiang University, Hangzhou, China
                [3 ] Model Animal Research Center and MOE Key Laboratory of Model Animals for Disease Study, Nanjing University, Nanjing, China
                [4 ] Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, United States of America
                The University of North Carolina at Chapel Hill, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-5807-4219
                Article
                PGENETICS-D-16-02709
                10.1371/journal.pgen.1006946
                5578494
                28859085
                1eebc950-3d23-47a7-b918-b33418f809be
                © 2017 Zhu et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 December 2016
                : 27 July 2017
                Page count
                Figures: 4, Tables: 0, Pages: 23
                Funding
                Funded by: Fundamental Research Funds for the Central Universities
                Award ID: 020814380070
                Award Recipient :
                Funded by: the National Basic Research Program of China
                Award ID: 2014CB542300
                Award Recipient :
                Funded by: the National Natural Science Foundation of China
                Award ID: 31271378
                Award Recipient :
                Funded by: the Natural Science Foundation of Jiangsu Province
                Award ID: BE2016737
                Award Recipient :
                This work was supported by: the National Basic Research Program of China (973 Program) (No. 2014CB542300) http://program.most.gov.cn/; the National Natural Science Foundation of China (Nos. 31271378 and 81250044) http://www.nsfc.gov.cn/; the Research Special Fund for Public Welfare Industry of Health (No. 201302018). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and life sciences
                Genetics
                Gene expression
                Gene regulation
                MicroRNAs
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Non-coding RNA
                MicroRNAs
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Honey Bees
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Pollen
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Experimental Organism Systems
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Agriculture
                Animal Products
                Honey
                Biology and Life Sciences
                Nutrition
                Diet
                Food
                Honey
                Medicine and Health Sciences
                Nutrition
                Diet
                Food
                Honey
                Research and analysis methods
                Extraction techniques
                RNA extraction
                Custom metadata
                All Illumina deep-sequencing files are available from the GEO database (accession number GSE76286).

                Genetics
                Genetics

                Comments

                Comment on this article