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Title: A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila

Journal Article · · PLoS Genetics
 [1];  [2];  [2];  [3];  [2];  [4];  [5];  [6];  [6];  [6];  [6];  [7];  [2]
  1. Univ. of California, Irvine, CA (United States). Dept. of Computer Science
  2. Harvard Medical School, Boston, MA (United States). Dept. of Systems Biology
  3. Harvard Univ., Cambridge, MA (United States). School of Engineering and Applied Sciences
  4. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences
  5. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Centre for Image Analysis
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics and Life Sciences Division
  7. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics and Life Sciences Division; Univ. of California, Berkeley, CA (United States). howard Hughes Medical Inst.
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Differences in the level, timing, or location of gene expression can contribute to alternative phenotypes at the molecular and organismal level. Understanding the origins of expression differences is complicated by the fact that organismal morphology and gene regulatory networks could potentially vary even between closely related species. To assess the scope of such changes, we used high-resolution imaging methods to measure mRNA expression in blastoderm embryos of Drosophila yakuba and Drosophila pseudoobscura and assembled these data into cellular resolution atlases, where expression levels for 13 genes in the segmentation network are averaged into species-specific, cellular resolution morphological frameworks. We demonstrate that the blastoderm embryos of these species differ in their morphology in terms of size, shape, and number of nuclei. We present an approach to compare cellular gene expression patterns between species, while accounting for varying embryo morphology, and apply it to our data and an equivalent dataset for Drosophila melanogaster. Our analysis reveals that all individual genes differ quantitatively in their spatio-temporal expression patterns between these species, primarily in terms of their relative position and dynamics. Despite many small quantitative differences, cellular gene expression profiles for the whole set of genes examined are largely similar. This suggests that cell types at this stage of development are conserved, though they can differ in their relative position by up to 3–4 cell widths and in their relative proportion between species by as much as 5-fold. Quantitative differences in the dynamics and relative level of a subset of genes between corresponding cell types may reflect altered regulatory functions between species. Our results emphasize that transcriptional networks can diverge over short evolutionary timescales and that even small changes can lead to distinct output in terms of the placement and number of equivalent cells.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627293
Journal Information:
PLoS Genetics, Vol. 7, Issue 10; ISSN 1553-7404
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (24)

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Novel approach to quantitative spatial gene expression uncovers genetic stochasticity in the developing Drosophila eye journal February 2019
Comparative studies of gene expression and the evolution of gene regulation journal June 2012
Evolution of Larval Segment Position across 12 Drosophila Species journal January 2019
An atlas of transcription factors expressed in the Drosophila melanogaster pupal terminalia posted_content January 2019
Evolution of larval segment position across 12 Drosophila species* journal January 2020
Quantitative comparison of the anterior-posterior patterning system in the embryos of five Drosophila species journal January 2018
A Digital Framework to Build, Visualize and Analyze a Gene Expression Atlas with Cellular Resolution in Zebrafish Early Embryogenesis journal June 2014
Modeling of the Dorsal Gradient across Species Reveals Interaction between Embryo Morphology and Toll Signaling Pathway during Evolution journal August 2014
Spatially varying cis-regulatory divergence in Drosophila embryos elucidates cis-regulatory logic journal November 2018
Depleting Gene Activities in Early Drosophila Embryos with the “Maternal-Gal4–shRNA” System journal January 2013
High-resolution gene expression data from blastoderm embryos of the scuttle fly Megaselia abdita journal March 2015
Quantitative Comparison of the Anterior-Posterior Patterning System in the Embryos of Five Drosophila Species journal July 2019
Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity journal January 2018
Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity journal June 2019
Reply to Jiang and Zhang: Parallel transcriptomic signature of monogamy: What is the null hypothesis anyway? journal August 2019
WholeCellViz: data visualization for whole-cell models journal January 2013
Spatially varying cis-regulatory divergence in Drosophila embryos elucidates cis-regulatory logic posted_content November 2017
Towards 3D in silico modeling of the sea urchin embryonic development journal September 2013
Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers journal March 2016
Shaped Singular Spectrum Analysis for Quantifying Gene Expression, with Application to the EarlyDrosophilaEmbryo journal January 2015
A novel procedure for absolute real-time quantification of gene expression patterns journal January 2012
Allele-specific expression elucidates cis-regulatory logic journal November 2018
Extensive divergence of transcription factor binding in Drosophila embryos with highly conserved gene expression text January 2013

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