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DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees

Foret, Sylvain; Kucharski, Robert; Pellegrini, Matteo; Feng, Suhua; Jacobsen, Steven E.; Robinson, Gene E; Maleszka, Ryszard

Description

In honey bees (Apis mellifera), the development of a larva into either a queen or worker depends on differential feeding with royal jelly and involves epigenomic modifications by DNA methyltransferases. To understand the role of DNA methylation in this process we sequenced the larval methylomes in both queens and workers. We show that the number of differentially methylated genes (DMGs) in larval head is significantly increased relative to adult brain (2,399 vs. 560) with more than 80% of DMGs...[Show more]

dc.contributor.authorForet, Sylvain
dc.contributor.authorKucharski, Robert
dc.contributor.authorPellegrini, Matteo
dc.contributor.authorFeng, Suhua
dc.contributor.authorJacobsen, Steven E.
dc.contributor.authorRobinson, Gene E
dc.contributor.authorMaleszka, Ryszard
dc.date.accessioned2015-12-10T23:20:16Z
dc.identifier.issn0027-8424
dc.identifier.urihttp://hdl.handle.net/1885/66250
dc.description.abstractIn honey bees (Apis mellifera), the development of a larva into either a queen or worker depends on differential feeding with royal jelly and involves epigenomic modifications by DNA methyltransferases. To understand the role of DNA methylation in this process we sequenced the larval methylomes in both queens and workers. We show that the number of differentially methylated genes (DMGs) in larval head is significantly increased relative to adult brain (2,399 vs. 560) with more than 80% of DMGs up-methylated in worker larvae. Several highly conserved metabolic and signaling pathways are enriched in methylated genes, underscoring the connection between dietary intake and metabolic flux. This includes genes related to juvenile hormone and insulin, two hormones shown previously to regulate caste determination. We also tie methylation data to expressional profiling and describe a distinct role for one of the DMGs encoding anaplastic lymphoma kinase (ALK), an important regulator of metabolism. We show that alk is not only differentially methylated and alternatively spliced in Apis, but also seems to be regulated by a cis-acting, anti-sense non- protein-coding transcript. The unusually complex regulation of ALK in Apis suggests that this protein could represent a previously unknown node in a process that activates downstream signaling according to a nutritional context. The correlation between methylation and alternative splicing of alk is consistent with the recently described mechanism involving RNA polymerase II pausing. Our study offers insights into diet-controlled development in Apis.
dc.publisherNational Academy of Sciences (USA)
dc.rightsAuthor/s retain copyright
dc.sourcePNAS - Proceedings of the National Academy of Sciences of the United States of America
dc.subjectKeywords: anaplastic lymphoma kinase; insulin; juvenile hormone; RNA polymerase II; article; dietary intake; DNA methylation; DNA splicing; gene expression profiling; honeybee; insect genome; larva; metabolic regulation; nonhuman; phenotype; priority journal; queen Polyphenism; Spliceosome; Ubiquitin
dc.titleDNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume109
dc.date.issued2012
local.identifier.absfor060404 - Epigenetics (incl. Genome Methylation and Epigenomics)
local.identifier.ariespublicationf5625xPUB1251
local.type.statusPublished Version
local.contributor.affiliationForet, Sylvain, College of Medicine, Biology and Environment, ANU
local.contributor.affiliationKucharski, Robert, College of Medicine, Biology and Environment, ANU
local.contributor.affiliationPellegrini, Matteo, University of California
local.contributor.affiliationFeng, Suhua, University of California
local.contributor.affiliationJacobsen, Steven E., University of California
local.contributor.affiliationRobinson, Gene E, University of Illinois
local.contributor.affiliationMaleszka, Ryszard, College of Medicine, Biology and Environment, ANU
local.bibliographicCitation.issue13
local.bibliographicCitation.startpage4968
local.bibliographicCitation.lastpage4973
local.identifier.doi10.1073/pnas.1202392109
local.identifier.absseo970106 - Expanding Knowledge in the Biological Sciences
dc.date.updated2016-02-24T08:41:47Z
local.identifier.scopusID2-s2.0-84859465140
local.identifier.thomsonID000302164200054
dcterms.accessRightsOpen Access
CollectionsANU Research Publications

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