Dataset Information

Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish.

ABSTRACT: Embryonic development of Austrofundulus limnaeus can occur along two phenotypic trajectories that are physiologically and biochemically distinct. Phenotype appears to be influenced by maternal provisioning based on the observation that young females produce predominately non-diapausing embryos and older females produce mostly diapausing embryos. Embryonic incubation temperature can override this pattern and alter trajectory. We hypothesized that temperature-induced phenotypic plasticity may be regulated by post-transcriptional modification via noncoding RNAs. As a first step to exploring this possibility, RNA-seq was used to generate transcriptomic profiles of small noncoding RNAs in embryos developing along the two alternative trajectories. We find distinct profiles of mature sequences belonging to the miR-10 family expressed in increasing abundance during development and mature sequences of miR-430 that follow the opposite pattern. Furthermore, miR-430 sequences are enriched in escape trajectory embryos. MiR-430 family members are known to target maternally provisioned mRNAs in zebrafish and may operate similarly in A. limnaeus in the context of normal development, and also by targeting trajectory-specific mRNAs. This expression pattern and function for miR-430 presents a potentially novel model for maternal-embryonic conflict in gene regulation that provides the embryo the ability to override maternal programming in the face of altered environmental conditions.

SUBMITTER: Romney ALT

PROVIDER: S-EPMC6127099 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish.

Romney Amie L T ALT Podrabsky Jason E JE

Scientific reports 20180906 1

Embryonic development of Austrofundulus limnaeus can occur along two phenotypic trajectories that are physiologically and biochemically distinct. Phenotype appears to be influenced by maternal provisioning based on the observation that young females produce predominately non-diapausing embryos and older females produce mostly diapausing embryos. Embryonic incubation temperature can override this pattern and alter trajectory. We hypothesized that temperature-induced phenotypic plasticity may be r ...[more]

PMID: 30190591

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Project description:BackgroundThe cellular signaling mechanisms and morphogenic movements involved in axis formation and gastrulation are well conserved between vertebrates. In nearly all described fish, gastrulation and the initial patterning of the embryonic axis occur concurrently with epiboly. However, annual killifish may be an exception to this norm. Annual killifish inhabit ephemeral ponds in South America and Africa and permanent populations persist by the production of stress-tolerant eggs. Early development of annual killifish is unique among vertebrates because their embryonic blastomeres disperse randomly across the yolk during epiboly and reaggregate several days later to form the embryo proper. In addition, annual killifish are able to arrest embryonic development in one to three stages, known as diapause I, II, and III. Little is known about how the highly conserved developmental signaling mechanisms associated with early vertebrate development may have shifted in order to promote the annual killifish phenotype. One of the most well-characterized and conserved transcription factors, oct4 (Pou5f1), may have a role in maintaining pluripotency. In contrast, BMP-antagonists such as chordin, noggin, and follistatin, have been previously shown to establish dorsal-ventral asymmetry during axis formation. Transcription factors from the SOXB1 group, such as sox2 and sox3, likely work to induce neural specification. Here, we determine the temporal expression of these developmental factors during embryonic development in the annual killifish Austrofundulus limnaeus using quantitative PCR and compare these patterns to other vertebrates.ResultsPartial transcript sequences to oct4, sox2, sox3, chordin, noggin-1, noggin-2, and follistatin were cloned, sequenced, and identified in A. limnaeus. We found oct4, sox3, chordin, and noggin-1 transcripts to likely be maternally inherited. Expression of sox2, follistatin, and noggin-2 transcripts were highest in stages following a visible embryonic axis.ConclusionsOur data suggest that embryonic cells acquire their germ layer identity following embryonic blastomere reaggregation in A. limnaeus. This process of cellular differentiation and axis formation may involve similar conserved signaling mechanisms to other vertebrates. We propose that the undifferentiated state is prolonged during blastomere dispersal, thus functioning as a developmental stress buffer prior to the establishment of embryonic asymmetry and positional identity among the embryonic cells.

Project description:BACKGROUND:African annual killifishes (Nothobranchius spp.) are adapted to seasonally desiccating habitats (ephemeral pools), surviving dry periods as dormant eggs. Given their peculiar life history, geographic aspects of their diversity uniquely combine patterns typical for freshwater taxa (river basin structure and elevation gradient) and terrestrial animals (rivers acting as major dispersal barriers). However, our current knowledge on fine-scale inter-specific and intra-specific genetic diversity of African annual fish is limited to a single, particularly dry region of their distribution (subtropical Mozambique). Using a widespread annual killifish from coastal Tanzania and Kenya, we tested whether the same pattern of genetic divergence pertains to a wet equatorial region in the centre of Nothobranchius distribution. RESULTS:In populations of Nothobranchius melanospilus species group across its range, we genotyped a part of mitochondrial cytochrome oxidase subunit 1 (COI) gene (83 individuals from 22 populations) and 10 nuclear microsatellite markers (251 individuals from 16 populations). We found five lineages with a clear phylogeographic structure but frequent secondary contact. Mitochondrial lineages were largely congruent with main population genetic clusters identified on microsatellite markers. In the upper Wami basin, populations are isolated as a putative Nothobranchius prognathus, but include also a population from a periphery of the middle Ruvu basin. Other four lineages (including putative Nothobranchius kwalensis) coexisted in secondary contact zones, but possessed clear spatial pattern. Main river channels did not form apparent barriers to dispersal. The most widespread lineage had strong signal of recent population expansion. CONCLUSIONS:We conclude that dispersal of a Nothobranchius species from a wet part of the genus distribution (tropical lowland) is not constrained by main river channels and closely related lineages frequently coexist in secondary contact zones. We also demonstrate contemporary connection between the Ruvu and Rufiji river basins. Our data do not provide genetic support for existence of recently described cryptic species from N. melanospilus complex, but cannot resolve this issue.

Dataset Information

Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish.

Publications

Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish.

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