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Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model.

ABSTRACT: The spatiotemporal control of gene expression is crucial for the successful completion of animal development. The evolutionary constraints on development are particularly strong for the mid-embryonic stage when body segments are specified, as evidenced by a high degree of morphological and protein-coding gene conservation during this period--a phenomenon known as the developmental hourglass. The discovery of microRNA-mediated gene control revealed an entirely new layer of complexity of the molecular networks that orchestrate development. However, the constraints on microRNA developmental expression and evolution, and the implications for animal evolution are less well understood. To systematically explore the conservation of microRNAs during development, we carried out a genome-wide comparative study of microRNA expression levels throughout the ontogenesis of two divergent fruit flies, Drosophila melanogaster and D. virilis. We show that orthologous microRNAs display highly similar temporal profiles regardless of their mutation rates, suggesting that the timely expression of microRNA genes can be more constrained than their sequence. Furthermore, transitions between key developmental events in the different species are accompanied by conserved shifts in microRNA expression profiles, with the mid-embryonic period between gastrulation and segmentation characterized by the highest similarity of microRNA expression. The conservation of microRNA expression therefore displays an hourglass pattern similar to that observed for protein-coding genes.

SUBMITTER: Ninova M

PROVIDER: S-EPMC4202322 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model.

Ninova Maria M Ronshaugen Matthew M Griffiths-Jones Sam S

Genome biology and evolution 20140827 9

The spatiotemporal control of gene expression is crucial for the successful completion of animal development. The evolutionary constraints on development are particularly strong for the mid-embryonic stage when body segments are specified, as evidenced by a high degree of morphological and protein-coding gene conservation during this period--a phenomenon known as the developmental hourglass. The discovery of microRNA-mediated gene control revealed an entirely new layer of complexity of the molec ...[more]

PMID: 25169982

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Project description:Circadian clocks are endogenous biochemical oscillators that control daily behavioral rhythms in all living organisms. In fruit fly, the circadian rhythms are typically studied using power spectra of multiday behavioral recordings. Despite decades of study, a quantitative understanding of the temporal shape of Drosophila locomotor rhythms is missing. Locomotor recordings have been used mostly to extract the period of the circadian clock, leaving these data-rich time series largely underutilized. The power spectra of Drosophila and mouse locomotion often show multiple peaks in addition to the expected at T ~ 24 h. Several theoretical and experimental studies have previously used these data to examine interactions between the circadian and other endogenous rhythms, in some cases, attributing peaks in the T < 24 h regime to ultradian oscillators. However, the analysis of fly locomotion was typically performed without considering the shape of time series, while the shape of the signal plays important role in its power spectrum. To account for locomotion patterns in circadian studies we construct a mathematical model of fly activity. Our model allows careful analysis of the temporal shape of behavioral recordings and can provide important information about biochemical mechanisms that control fly activity.Here we propose a mathematical model with four exponential terms and a single period of oscillation that closely reproduces the shape of the locomotor data in both time and frequency domains. Using our model, we reexamine interactions between the circadian and other endogenous rhythms and show that the proposed single-period waveform is sufficient to explain the position and height of >88 % of spectral peaks in the locomotion of wild-type and circadian mutants of Drosophila. In the time domain, we find the timescales of the exponentials in our model to be ~1.5 h(-1) on average.Our results indicate that multiple spectral peaks from fly locomotion are simply harmonics of the circadian period rather than independent ultradian oscillators as previously reported. From timescales of the exponentials we hypothesize that model rates reflect activity of the neuropeptides that likely transduce signals of the circadian clock and the sleep-wake homeostat to shape behavioral outputs.

Project description:The M-bM-^@M-^Xdevelopmental hourglassM-bM-^@M-^Y concept suggests that intermediate developmental stages are most resistant to evolutionary changes and that differences between species arise through divergence later in development. This high conservation during mid-development is illustrated by the M-bM-^@M-^XwaistM-bM-^@M-^Y of the hourglass and it represents a low probability of evolutionary change. Earlier molecular surveys both on animals and plants have shown that the genes expressed at the waist stage are more ancient and more conserved in their expression. The existence of such a developmental hourglass has not been explored in fungi, another eukaryotic kingdom. In this study, we generated a series of transcriptomic data covering the entire lifecycle of a model mushroom-forming fungus, Coprinopsis cinerea, and we observed a molecular hourglass over its development. The M-bM-^@M-^Xyoung fruiting bodyM-bM-^@M-^Y (YFB) is the stage that expresses the evolutionarily oldest (lowest transcriptome age index, TAI) transcriptome and gives the strongest signal of purifying selection (lowest transcriptome divergence index, TDI). We also demonstrated that all three kingdoms M-bM-^@M-^S animals, plants and fungi M-bM-^@M-^S display high expression levels of genes in M-bM-^@M-^Xinformation storage and processingM-bM-^@M-^Y at the waist stages, whereas the genes in M-bM-^@M-^XmetabolismM-bM-^@M-^Y become more highly expressed later. Besides, the three kingdoms all show underrepresented M-bM-^@M-^Xsignal transductionM-bM-^@M-^Y at the waist stages. The synchronic existence of a molecular M-bM-^@M-^XhourglassM-bM-^@M-^Y across the three kingdoms reveals a mutual strategy for eukaryotes to incorporate evolutionary innovations. NimbleGen custom microarray with total RNAs extracted from two biological replicates for each stage of mycelium, fruiting initials (~2mm tall), stage 2 primordium (~1cm tall), young fruiting body (~2cm tall) and the fully-expanded cap of the mature fruiting body (~4cm tall). Mycelia from 5 agar plates were collected and pooled to form one replicate. For the other stages, 4-5 independent structures were isolated and their RNA extracted as one replicate sample.

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Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model.

Publications

Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model.

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