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Genome-wide transcriptome profiling and spatial expression analyses identify signals and switches of development in tapeworms.

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cam.issuedOnline2018-11-09
dc.contributor.authorOlson, Peter D
dc.contributor.authorZarowiecki, Magdalena
dc.contributor.authorJames, Katherine
dc.contributor.authorBaillie, Andrew
dc.contributor.authorBartl, Georgie
dc.contributor.authorBurchell, Phil
dc.contributor.authorChellappoo, Azita
dc.contributor.authorJarero, Francesca
dc.contributor.authorTan, Li Ying
dc.contributor.authorHolroyd, Nancy
dc.contributor.authorBerriman, Matt
dc.date.accessioned2018-11-10T07:02:31Z
dc.date.available2018-11-10T07:02:31Z
dc.date.issued2018
dc.date.updated2018-11-10T07:02:28Z
dc.description.abstractBACKGROUND: Tapeworms are agents of neglected tropical diseases responsible for significant health problems and economic loss. They also exhibit adaptations to a parasitic lifestyle that confound comparisons of their development with other animals. Identifying the genetic factors regulating their complex ontogeny is essential to understanding unique aspects of their biology and for advancing novel therapeutics. Here we use RNA sequencing to identify up-regulated signalling components, transcription factors and post-transcriptional/translational regulators (genes of interest, GOI) in the transcriptomes of Larvae and different regions of segmented worms in the tapeworm Hymenolepis microstoma and combine this with spatial gene expression analyses of a selection of genes. RESULTS: RNA-seq reads collectively mapped to 90% of the > 12,000 gene models in the H. microstoma v.2 genome assembly, demonstrating that the transcriptome profiles captured a high percentage of predicted genes. Contrasts made between the transcriptomes of Larvae and whole, adult worms, and between the Scolex-Neck, mature strobila and gravid strobila, resulted in 4.5-30% of the genes determined to be differentially expressed. Among these, we identified 190 unique GOI up-regulated in one or more contrasts, including a large range of zinc finger, homeobox and other transcription factors, components of Wnt, Notch, Hedgehog and TGF-β/BMP signalling, and post-transcriptional regulators (e.g. Boule, Pumilio). Heatmap clusterings based on overall expression and on select groups of genes representing 'signals' and 'switches' showed that expression in the Scolex-Neck region is more similar to that of Larvae than to the mature or gravid regions of the adult worm, which was further reflected in large overlap of up-regulated GOI. CONCLUSIONS: Spatial expression analyses in Larvae and adult worms corroborated inferences made from quantitative RNA-seq data and in most cases indicated consistency with canonical roles of the genes in other animals, including free-living flatworms. Recapitulation of developmental factors up-regulated during larval metamorphosis suggests that strobilar growth involves many of the same underlying gene regulatory networks despite the significant disparity in developmental outcomes. The majority of genes identified were investigated in tapeworms for the first time, setting the stage for advancing our understanding of developmental genetics in an important group of flatworm parasites.
dc.identifier.citationEvoDevo. 2018 Nov 09;9(1):21
dc.identifier.doi10.17863/CAM.32275
dc.identifier.eissn2041-9139
dc.identifier.issn2041-9139
dc.identifier.urihttps://www.repository.cam.ac.uk/handle/1810/284905
dc.language.isoeng
dc.language.rfc3066en
dc.publisherSpringer Science and Business Media LLC
dc.publisher.urlhttp://dx.doi.org/10.1186/s13227-018-0110-5
dc.rights.holderThe Author(s)
dc.subjectDifferential gene expression
dc.subjectHymenolepis
dc.subjectPost-transcriptional regulators
dc.subjectRNA-seq
dc.subjectSignalling factors
dc.subjectTapeworms
dc.subjectTranscription factors
dc.subjectTranscriptomics
dc.titleGenome-wide transcriptome profiling and spatial expression analyses identify signals and switches of development in tapeworms.
dc.typeJournal Article
dcterms.dateAccepted2018-10-05
prism.publicationNameEvodevo
rioxxterms.versionofrecord10.1186/s13227-018-0110-5

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