A “Developmental Hourglass” in Fungi

AbstractCombining transcriptome data of biological processes or response to stimuli with evolutionary information such as the phylogenetic conservation of genes or their sequence divergence rates enables the investigation of evolutionary constraints on these processes or responses. Such phylotranscriptomic analyses recently unraveled that mid-developmental transcriptomes of fly, fish, and cress were dominated by evolutionarily conserved genes and genes under negative selection and thus recapitulated the developmental hourglass on the transcriptomic level. Here, we present a protocol for performing phylotranscriptomic analyses on any biological process of interest. When applying this protocol, users are capable of detecting different evolutionary constraints acting on different stages of the biological process of interest in any species. For each step of the protocol, modular and easy-to-use open-source software tools are provided, which enable a broad range of scientists to apply phylotranscriptomic analyses to a wide spectrum of biological questions.

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The developmental hourglass model: a predictor of the basic body plan?

Development ◽

10.1242/dev.107318 ◽

2014 ◽

Vol 141 (24) ◽

pp. 4649-4655 ◽

Cited By ~ 65

Author(s):

N. Irie ◽

S. Kuratani

Keyword(s):

Body Plan ◽

Basic Body ◽

Hourglass Model ◽

Developmental Hourglass

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Conserved Temporal Patterns of MicroRNA Expression in Drosophila Support a Developmental Hourglass Model

Genome Biology and Evolution ◽

10.1093/gbe/evu183 ◽

2014 ◽

Vol 6 (9) ◽

pp. 2459-2467 ◽

Cited By ~ 16

Author(s):

Maria Ninova ◽

Matthew Ronshaugen ◽

Sam Griffiths-Jones

Keyword(s):

Temporal Patterns ◽

Microrna Expression ◽

Hourglass Model ◽

Developmental Hourglass

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The hourglass model of evolutionary conservation during embryogenesis extends to developmental enhancers with signatures of positive selection

10.1101/2020.11.02.364505 ◽

2020 ◽

Author(s):

Jialin Liu ◽

Rebecca R. Viales ◽

Pierre Khoueiry ◽

James P. Reddington ◽

Charles Girardot ◽

...

Keyword(s):

Gene Expression ◽

Positive Selection ◽

Evolutionary Conservation ◽

Animal Evolution ◽

Species Comparisons ◽

Underlying Mechanisms ◽

Hourglass Model ◽

Late Stages ◽

Developmental Hourglass

Inter-species comparisons of both morphology and gene expression within a phylum have revealed a period in the middle of embryogenesis with more similarity between species compared to earlier and later time-points. This developmental hourglass pattern has been observed in many phyla, yet the evolutionary constraints on gene expression, and underlying mechanisms of how this is regulated, remains elusive. Moreover, the role of positive selection on gene regulation in the more diverged earlier and later stages of embryogenesis remains unknown. Here, using DNase-seq to identify regulatory regions in two distant Drosophila species (D. melanogaster and D. virilis), we assessed the evolutionary conservation and adaptive evolution of enhancers throughout multiple stages of embryogenesis. This revealed a higher proportion of conserved enhancers at the phylotypic period, providing a regulatory basis for the hourglass expression pattern. Using an in silico mutagenesis approach, we detect signatures of positive selection on developmental enhancers at early and late stages of embryogenesis, with a depletion at the phylotypic period, suggesting positive selection as one evolutionary mechanism underlying the hourglass pattern of animal evolution.

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Post-embryonic hourglass patterns mark ontogenetic transitions in plant development

10.1101/035527 ◽

2015 ◽

Author(s):

Hajk-Georg Drost ◽

Julia Bellstaedt ◽

Diarmuid O'Maoileidigh ◽

Anderson Silva ◽

Alexander Gabel ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Life Cycle ◽

Flower Development ◽

Reproductive Development ◽

Body Plan ◽

Phase Changes ◽

Morphological Pattern ◽

Model Plant Arabidopsis Thaliana ◽

Developmental Hourglass ◽

Plant Arabidopsis Thaliana

The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found post-embryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints.

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Somite number and vertebrate evolution

Development ◽

10.1242/dev.125.2.151 ◽

1998 ◽

Vol 125 (2) ◽

pp. 151-160 ◽

Cited By ~ 5

Author(s):

M.K. Richardson ◽

S.P. Allen ◽

G.M. Wright ◽

A. Raynaud ◽

J. Hanken

Keyword(s):

Expression Patterns ◽

Vertebrate Evolution ◽

Pharyngeal Arches ◽

Evolution And Development ◽

Evolutionary Changes ◽

Phylotypic Stage ◽

Tailbud Stage ◽

Hourglass Model ◽

Somite Number ◽

Developmental Hourglass

Variation in segment number is an important but neglected feature of vertebrate evolution. Some vertebrates have as few as six trunk vertebrae, while others have hundreds. We examine this phenomenon in relation to recent models of evolution and development. Surprisingly, differences in vertebral number are foreshadowed by different somite counts at the tailbud stage, thought to be a highly conserved (phylotypic) stage. Somite number therefore violates the ‘developmental hourglass’ model. We argue that this is because somitogenesis shows uncoupling or dissociation from the conserved positional field encoded by genes of the zootype. Several other systems show this kind of dissociation, including limbs and feathers. Bmp-7 expression patterns demonstrate dissociation in the chick pharyngeal arches. This makes it difficult to recognise a common stage of pharyngeal development or ‘pharyngula’ in all species. Rhombomere number is more stable during evolution than somite number, possibly because segmentation and positional specification in the hindbrain are relatively interdependent. Although developmental mechanisms are strongly conserved, dissociation allows at least some major evolutionary changes to be generated in phylotypic stages.

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