A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila
Abstract
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 cellmore »
- Authors:
-
- Univ. of California, Irvine, CA (United States). Dept. of Computer Science
- Harvard Medical School, Boston, MA (United States). Dept. of Systems Biology
- Harvard Univ., Cambridge, MA (United States). School of Engineering and Applied Sciences
- Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences
- Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Centre for Image Analysis
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics and Life Sciences Division
- 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.
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1627293
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 10; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Genetics & Heredity
Citation Formats
Fowlkes, Charless C., Eckenrode, Kelly B., Bragdon, Meghan D., Meyer, Miriah, Wunderlich, Zeba, Simirenko, Lisa, Luengo Hendriks, Cris L., Keränen, Soile V. E., Henriquez, Clara, Knowles, David W., Biggin, Mark D., Eisen, Michael B., and DePace, Angela H. A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila. United States: N. p., 2011.
Web. doi:10.1371/journal.pgen.1002346.
Fowlkes, Charless C., Eckenrode, Kelly B., Bragdon, Meghan D., Meyer, Miriah, Wunderlich, Zeba, Simirenko, Lisa, Luengo Hendriks, Cris L., Keränen, Soile V. E., Henriquez, Clara, Knowles, David W., Biggin, Mark D., Eisen, Michael B., & DePace, Angela H. A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila. United States. https://doi.org/10.1371/journal.pgen.1002346
Fowlkes, Charless C., Eckenrode, Kelly B., Bragdon, Meghan D., Meyer, Miriah, Wunderlich, Zeba, Simirenko, Lisa, Luengo Hendriks, Cris L., Keränen, Soile V. E., Henriquez, Clara, Knowles, David W., Biggin, Mark D., Eisen, Michael B., and DePace, Angela H. Thu .
"A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila". United States. https://doi.org/10.1371/journal.pgen.1002346. https://www.osti.gov/servlets/purl/1627293.
@article{osti_1627293,
title = {A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila},
author = {Fowlkes, Charless C. and Eckenrode, Kelly B. and Bragdon, Meghan D. and Meyer, Miriah and Wunderlich, Zeba and Simirenko, Lisa and Luengo Hendriks, Cris L. and Keränen, Soile V. E. and Henriquez, Clara and Knowles, David W. and Biggin, Mark D. and Eisen, Michael B. and DePace, Angela H.},
abstractNote = {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.},
doi = {10.1371/journal.pgen.1002346},
journal = {PLoS Genetics},
number = 10,
volume = 7,
place = {United States},
year = {Thu Oct 27 00:00:00 EDT 2011},
month = {Thu Oct 27 00:00:00 EDT 2011}
}
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Works referenced in this record:
From elements to modules: regulatory evolution in Ascomycota fungi
journal, December 2009
- Wohlbach, Dana J.; Thompson, Dawn Anne; Gasch, Audrey P.
- Current Opinion in Genetics & Development, Vol. 19, Issue 6
Wasps, beetles and the beginning of the ends
journal, January 2006
- McGregor, Alistair P.
- BioEssays, Vol. 28, Issue 7
Evolution and Inheritance of Early Embryonic Patterning in Drosophila Simulans and d. Sechellia: Patterning Variation in Drosphila Simulans and d. Sechellia
journal, December 2010
- Lott, Susan E.; Ludwig, Michael Z.; Kreitman, Martin
- Evolution, Vol. 65, Issue 5
Three-dimensional morphology and gene expression in the Drosophilablastoderm at cellular resolution I: data acquisition pipeline
journal, January 2006
- Luengo Hendriks, Cris L.; Keranen, Soile V. E.; Fowlkes, Charless C.
- Genome Biology, Vol. 7, Issue 12, p. R123
Sepsid even-skipped Enhancers Are Functionally Conserved in Drosophila Despite Lack of Sequence Conservation
journal, June 2008
- Hare, Emily E.; Peterson, Brant K.; Iyer, Venky N.
- PLoS Genetics, Vol. 4, Issue 6
Three-dimensional morphology and gene expression in the Drosophilablastoderm at cellular resolution II: dynamics
journal, January 2006
- Keranen, Soile V. E.; Fowlkes, Charless C.; Luengo Hendriks, Cris L.
- Genome Biology, Vol. 7, Issue 12, p. R124
Gene Regulation at the Single-Cell Level
journal, March 2005
- Rosenfeld, N.
- Science, Vol. 307, Issue 5717
Evolution of Gene Regulatory Networks Controlling Body Plan Development
journal, March 2011
- Peter, Isabelle S.; Davidson, Eric H.
- Cell, Vol. 144, Issue 6
Genome-wide analysis of promoter architecture in Drosophila melanogaster
journal, December 2010
- Hoskins, R. A.; Landolin, J. M.; Brown, J. B.
- Genome Research, Vol. 21, Issue 2
Dynamic reprogramming of chromatin accessibility during Drosophila embryo development
journal, January 2011
- Thomas, Sean; Li, Xiao-Yong; Sabo, Peter J.
- Genome Biology, Vol. 12, Issue 5
Single-cell genomics
journal, March 2011
- Kalisky, Tomer; Quake, Stephen R.
- Nature Methods, Vol. 8, Issue 4
Gene expression divergence recapitulates the developmental hourglass model
journal, December 2010
- Kalinka, Alex T.; Varga, Karolina M.; Gerrard, Dave T.
- Nature, Vol. 468, Issue 7325
Meeting report: First light sheet based fluorescence microscopy workshop
journal, August 2010
- Reynaud, Emmanuel G.; Tomancak, Pavel
- Biotechnology Journal, Vol. 5, Issue 8
The evolutionary significance of cis-regulatory mutations
journal, March 2007
- Wray, Gregory A.
- Nature Reviews Genetics, Vol. 8, Issue 3
Plasticity of the cis-Regulatory Input Function of a Gene
journal, March 2006
- Mayo, Avraham E.; Setty, Yaakov; Shavit, Seagull
- PLoS Biology, Vol. 4, Issue 4
Giant, Krüppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo
journal, March 2010
- Wilson, Megan J.; Havler, Melanie; Dearden, Peter K.
- Developmental Biology, Vol. 339, Issue 1
A Quantitative Spatiotemporal Atlas of Gene Expression in the Drosophila Blastoderm
journal, April 2008
- Fowlkes, Charless C.; Hendriks, Cris L. Luengo; Keränen, Soile V. E.
- Cell, Vol. 133, Issue 2
Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution
journal, July 2008
- Carroll, Sean B.
- Cell, Vol. 134, Issue 1
Evolution Acts on Enhancer Organization to Fine-Tune Gradient Threshold Readouts
journal, November 2008
- Crocker, Justin; Tamori, Yoichiro; Erives, Albert
- PLoS Biology, Vol. 6, Issue 11
Selective plane illumination microscopy techniques in developmental biology
journal, May 2009
- Huisken, J.; Stainier, D. Y. R.
- Development, Vol. 136, Issue 12
Comparative genomics of gene regulation—conservation and divergence of cis-regulatory information
journal, December 2009
- Meireles-Filho, Antonio CA; Stark, Alexander
- Current Opinion in Genetics & Development, Vol. 19, Issue 6
Intraspecific Polymorphism to Interspecific Divergence: Genetics of Pigmentation in Drosophila
journal, October 2009
- Wittkopp, P. J.; Stewart, E. E.; Arnold, L. L.
- Science, Vol. 326, Issue 5952
Life‐History Consequences of Divergent Selection on Egg Size in Drosophila melanogaster
journal, September 1999
- Schwarzkopf, Lin; Blows, Mark W.; Caley, M. Julian
- The American Naturalist, Vol. 154, Issue 3
Deciphering a transcriptional regulatory code: modeling short‐range repression in the Drosophila embryo
journal, January 2010
- Fakhouri, Walid D.; Ay, Ahmet; Sayal, Rupinder
- Molecular Systems Biology, Vol. 6, Issue 1
Registering Drosophila embryos at cellular resolution to build a quantitative 3D atlas of gene expression patterns and morphology
conference, January 2005
- Fowlkes, C. C.; Luengo Hendriks, C. L.; Keranen, S. V. E.
- 2005 IEEE Computational Systems Bioinformatics Conference Workshops and Poster Abstracts, 2005 IEEE Computational Systems Bioinformatics Conference - Workshops (CSBW'05)
Artificial Selection on egg size Perturbs Early Pattern Formation in Drosophila Melanogaster: Selection Perturbs eve Stripe Border Positions
journal, July 2010
- Miles, Cecelia M.; Lott, Susan E.; Luengo Hendriks, Cris L.
- Evolution, Vol. 65, Issue 1
Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene
journal, September 2006
- Janssens, Hilde; Hou, Shuling; Jaeger, Johannes
- Nature Genetics, Vol. 38, Issue 10
The Developmental Role of Agouti in Color Pattern Evolution
journal, February 2011
- Manceau, M.; Domingues, V. S.; Mallarino, R.
- Science, Vol. 331, Issue 6020
Predicting expression patterns from regulatory sequence in Drosophila segmentation
journal, January 2008
- Segal, Eran; Raveh-Sadka, Tali; Schroeder, Mark
- Nature, Vol. 451, Issue 7178
Evolution of Regulatory Sequences in 12 Drosophila Species
journal, January 2009
- Kim, Jaebum; He, Xin; Sinha, Saurabh
- PLoS Genetics, Vol. 5, Issue 1
Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos
journal, November 2004
- Goltsev, Yury; Hsiong, William; Lanzaro, Gregory
- Developmental Biology, Vol. 275, Issue 2
Thermal Evolution of Egg Size in Drosophila melanogaster
journal, December 1996
- Azevedo, Ricardo B. R.; French, Vernon; Partridge, Linda
- Evolution, Vol. 50, Issue 6
Adaptive Evolution of Pelvic Reduction in Sticklebacks by Recurrent Deletion of a Pitx1 Enhancer
journal, December 2009
- Chan, Y. F.; Marks, M. E.; Jones, F. C.
- Science, Vol. 327, Issue 5963
Microevolutionary Divergence Pattern of the Segmentation Gene hunchback in Drosophila
journal, November 1998
- Tautz, D.; Nigro, L.
- Molecular Biology and Evolution, Vol. 15, Issue 11
The gap gene network
journal, October 2010
- Jaeger, Johannes
- Cellular and Molecular Life Sciences, Vol. 68, Issue 2
Binding Site Turnover Produces Pervasive Quantitative Changes in Transcription Factor Binding between Closely Related Drosophila Species
journal, March 2010
- Bradley, Robert K.; Li, Xiao-Yong; Trapnell, Cole
- PLoS Biology, Vol. 8, Issue 3
Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence
journal, December 2010
- Berezikov, E.; Robine, N.; Samsonova, A.
- Genome Research, Vol. 21, Issue 2
Pathline: A Tool For Comparative Functional Genomics
journal, June 2010
- Meyer, M.; Wong, B.; Styczynski, M.
- Computer Graphics Forum, Vol. 29, Issue 3
Maternal activation of gap genes in the hover fly Episyrphus
journal, April 2010
- Lemke, S.; Busch, S. E.; Antonopoulos, D. A.
- Development, Vol. 137, Issue 10
Thermodynamics-Based Models of Transcriptional Regulation by Enhancers: The Roles of Synergistic Activation, Cooperative Binding and Short-Range Repression
journal, September 2010
- He, Xin; Samee, Md. Abul Hassan; Blatti, Charles
- PLoS Computational Biology, Vol. 6, Issue 9
Heads and tails: Evolution of antero-posterior patterning in insects
journal, April 2009
- Rosenberg, Miriam I.; Lynch, Jeremy A.; Desplan, Claude
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1789, Issue 4
Functional Evolution of a cis-Regulatory Module
journal, March 2005
- Ludwig, Michael Z.; Palsson, Arnar; Alekseeva, Elena
- PLoS Biology, Vol. 3, Issue 4
Regulatory Divergence in Drosophila melanogaster and D. simulans , a Genomewide Analysis of Allele-Specific Expression
journal, August 2009
- Graze, Rita M.; McIntyre, Lauren M.; Main, Bradley J.
- Genetics, Vol. 183, Issue 2
Does Positive Selection Drive Transcription Factor Binding Site Turnover? A Test with Drosophila Cis-Regulatory Modules
journal, April 2011
- He, Bin Z.; Holloway, Alisha K.; Maerkl, Sebastian J.
- PLoS Genetics, Vol. 7, Issue 4
How to make stripes: deciphering the transition from non-periodic to periodic patterns in Drosophila segmentation
journal, June 2011
- Schroeder, M. D.; Greer, C.; Gaul, U.
- Development, Vol. 138, Issue 14
Molecular heterochrony in the early development of Drosophila
journal, January 2000
- Kim, J.; Kerr, J. Q.; Min, G. -S.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 1
Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions
journal, January 2009
- MacArthur, Stewart; Li, Xiao-Yong; Li, Jingyi
- Genome Biology, Vol. 10, Issue 7
Divergent structure and function of the bicoid gene in Muscoidea fly species
journal, July 2001
- Shaw, Philip J.; Salameh, Ahmad; McGregor, Alistair P.
- Evolution and Development, Vol. 3, Issue 4
Changes in Selective Effects Over Time Facilitate Turnover of Enhancer Sequences
journal, November 2010
- Bullaughey, Kevin
- Genetics, Vol. 187, Issue 2
Two new roles for the Drosophila AP patterning system in early morphogenesis
journal, December 2001
- Blankenship, J. Todd; Wieschaus, Eric
- Development, Vol. 128, Issue 24
Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration
journal, April 1997
- Namba, R.; Pazdera, T. M.; Cerrone, R. L.
- Development, Vol. 124, Issue 7
Wasps, beetles and the beginning of the ends
journal, January 2006
- McGregor, Alistair P.
- BioEssays, Vol. 28, Issue 7
The gap gene network
journal, October 2010
- Jaeger, Johannes
- Cellular and Molecular Life Sciences, Vol. 68, Issue 2
Zebra patterns in fly embryos: Activation of stripes or repression of interstripes?
journal, January 1990
- Carroll, Sean B.
- Cell, Vol. 60, Issue 1
The origin of pattern and polarity in the Drosophila embryo
journal, January 1992
- Johnston, Daniel St; Nüsslein-Volhard, Christiane
- Cell, Vol. 68, Issue 2
Heads and tails: Evolution of antero-posterior patterning in insects
journal, April 2009
- Rosenberg, Miriam I.; Lynch, Jeremy A.; Desplan, Claude
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1789, Issue 4
A Quantitative Spatiotemporal Atlas of Gene Expression in the Drosophila Blastoderm
journal, April 2008
- Fowlkes, Charless C.; Hendriks, Cris L. Luengo; Keränen, Soile V. E.
- Cell, Vol. 133, Issue 2
Comparative genomics of gene regulation—conservation and divergence of cis-regulatory information
journal, December 2009
- Meireles-Filho, Antonio CA; Stark, Alexander
- Current Opinion in Genetics & Development, Vol. 19, Issue 6
Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos
journal, November 2004
- Goltsev, Yury; Hsiong, William; Lanzaro, Gregory
- Developmental Biology, Vol. 275, Issue 2
Giant, Krüppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo
journal, March 2010
- Wilson, Megan J.; Havler, Melanie; Dearden, Peter K.
- Developmental Biology, Vol. 339, Issue 1
Deciphering a transcriptional regulatory code: modeling short‐range repression in the Drosophila embryo
journal, January 2010
- Fakhouri, Walid D.; Ay, Ahmet; Sayal, Rupinder
- Molecular Systems Biology, Vol. 6, Issue 1
Morphological evolution through multiple cis-regulatory mutations at a single gene
journal, July 2007
- McGregor, Alistair P.; Orgogozo, Virginie; Delon, Isabelle
- Nature, Vol. 448, Issue 7153
Predicting expression patterns from regulatory sequence in Drosophila segmentation
journal, January 2008
- Segal, Eran; Raveh-Sadka, Tali; Schroeder, Mark
- Nature, Vol. 451, Issue 7178
Gene expression divergence recapitulates the developmental hourglass model
journal, December 2010
- Kalinka, Alex T.; Varga, Karolina M.; Gerrard, Dave T.
- Nature, Vol. 468, Issue 7325
Single-cell genomics
journal, March 2011
- Kalisky, Tomer; Quake, Stephen R.
- Nature Methods, Vol. 8, Issue 4
Divergent structure and function of the bicoid gene in Muscoidea fly species
journal, July 2001
- Shaw, Philip J.; Salameh, Ahmad; McGregor, Alistair P.
- Evolution and Development, Vol. 3, Issue 4
Molecular heterochrony in the early development of Drosophila
journal, January 2000
- Kim, J.; Kerr, J. Q.; Min, G. -S.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 1
Life‐History Consequences of Divergent Selection on Egg Size in Drosophila melanogaster
journal, September 1999
- Schwarzkopf, Lin; Blows, Mark W.; Caley, M. Julian
- The American Naturalist, Vol. 154, Issue 3
Microevolutionary Divergence Pattern of the Segmentation Gene hunchback in Drosophila
journal, November 1998
- Tautz, D.; Nigro, L.
- Molecular Biology and Evolution, Vol. 15, Issue 11
MulteeSum: A Tool for Comparative Spatial and Temporal Gene Expression Data
journal, November 2010
- Meyer, M.; Munzner, T.; DePace, A.
- IEEE Transactions on Visualization and Computer Graphics, Vol. 16, Issue 6
bicoid occurrence and Bicoid-dependent hunchback regulation in lower cyclorrhaphan flies
journal, July 2008
- Lemke, Steffen; Stauber, Michael; Shaw, Philip J.
- Evolution & Development, Vol. 10, Issue 4
Intraspecific Polymorphism to Interspecific Divergence: Genetics of Pigmentation in Drosophila
journal, October 2009
- Wittkopp, P. J.; Stewart, E. E.; Arnold, L. L.
- Science, Vol. 326, Issue 5952
The Developmental Role of Agouti in Color Pattern Evolution
journal, February 2011
- Manceau, M.; Domingues, V. S.; Mallarino, R.
- Science, Vol. 331, Issue 6020
Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions
journal, January 2009
- MacArthur, Stewart; Li, Xiao-Yong; Li, Jingyi
- Genome Biology, Vol. 10, Issue 7
Dynamic reprogramming of chromatin accessibility during Drosophila embryo development
journal, January 2011
- Thomas, Sean; Li, Xiao-Yong; Sabo, Peter J.
- Genome Biology, Vol. 12, Issue 5
Selective plane illumination microscopy techniques in developmental biology
journal, May 2009
- Huisken, J.; Stainier, D. Y. R.
- Development, Vol. 136, Issue 12
Maternal activation of gap genes in the hover fly Episyrphus
journal, April 2010
- Lemke, S.; Busch, S. E.; Antonopoulos, D. A.
- Development, Vol. 137, Issue 10
Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration
journal, April 1997
- Namba, R.; Pazdera, T. M.; Cerrone, R. L.
- Development, Vol. 124, Issue 7
Two new roles for the Drosophila AP patterning system in early morphogenesis
journal, December 2001
- Blankenship, J. Todd; Wieschaus, Eric
- Development, Vol. 128, Issue 24
Automatic channel unmixing for high-throughput quantitative analysis of fluorescence images
journal, January 2007
- Luengo Hendriks, Cris L.; Keränen, Soile V.; Biggin, Mark D.
- Optics Express, Vol. 15, Issue 19
Functional Evolution of a cis-Regulatory Module
journal, March 2005
- Ludwig, Michael Z.; Palsson, Arnar; Alekseeva, Elena
- PLoS Biology, Vol. 3, Issue 4
Mutations Change the Boolean Logic of Gene Regulation
journal, March 2006
- Robinson, Richard
- PLoS Biology, Vol. 4, Issue 4
Evolution Acts on Enhancer Organization to Fine-Tune Gradient Threshold Readouts
journal, November 2008
- Crocker, Justin; Tamori, Yoichiro; Erives, Albert
- PLoS Biology, Vol. 6, Issue 11
Thermodynamics-Based Models of Transcriptional Regulation by Enhancers: The Roles of Synergistic Activation, Cooperative Binding and Short-Range Repression
journal, September 2010
- He, Xin; Samee, Md. Abul Hassan; Blatti, Charles
- PLoS Computational Biology, Vol. 6, Issue 9
Sepsid even-skipped Enhancers Are Functionally Conserved in Drosophila Despite Lack of Sequence Conservation
journal, June 2008
- Hare, Emily E.; Peterson, Brant K.; Iyer, Venky N.
- PLoS Genetics, Vol. 4, Issue 6
Regulatory Divergence in Drosophila melanogaster and D. simulans , a Genomewide Analysis of Allele-Specific Expression
journal, August 2009
- Graze, Rita M.; McIntyre, Lauren M.; Main, Bradley J.
- Genetics, Vol. 183, Issue 2
Changes in Selective Effects Over Time Facilitate Turnover of Enhancer Sequences
journal, November 2010
- Bullaughey, Kevin
- Genetics, Vol. 187, Issue 2
Works referencing / citing this record:
Novel approach to quantitative spatial gene expression uncovers genetic stochasticity in the developing Drosophila eye
posted_content, March 2018
- Ali, Sammi; Signor, Sarah A.; Kozlov, Konstantin
- Evolution & Development
Novel approach to quantitative spatial gene expression uncovers genetic stochasticity in the developing Drosophila eye
journal, February 2019
- Ali, Sammi; Signor, Sarah A.; Kozlov, Konstantin
- Evolution & Development, Vol. 21, Issue 3
Comparative studies of gene expression and the evolution of gene regulation
journal, June 2012
- Romero, Irene Gallego; Ruvinsky, Ilya; Gilad, Yoav
- Nature Reviews Genetics, Vol. 13, Issue 7
Evolution of Larval Segment Position across 12 Drosophila Species
journal, January 2019
- Kalay, Gizem; Atallah, Joel; Sierra, Noemie C.
- Evolution
An atlas of transcription factors expressed in the Drosophila melanogaster pupal terminalia
posted_content, January 2019
- Vincent, Ben J.; Rice, Gavin R.; Wong, Gabriella M.
- BioRxiv
Evolution of larval segment position across 12 Drosophila species*
journal, January 2020
- Kalay, Gizem; Atallah, Joel; Sierra, Noemie C.
- Evolution, Vol. 74, Issue 7
Quantitative comparison of the anterior-posterior patterning system in the embryos of five Drosophila species
journal, January 2018
- Wunderlich, Zeba; Fowlkes, Charless C.; Eckenrode, Kelly B.
- G3: Genes|Genomes|Genetics
A Digital Framework to Build, Visualize and Analyze a Gene Expression Atlas with Cellular Resolution in Zebrafish Early Embryogenesis
journal, June 2014
- Castro-González, Carlos; Luengo-Oroz, Miguel A.; Duloquin, Louise
- PLoS Computational Biology, Vol. 10, Issue 6
Modeling of the Dorsal Gradient across Species Reveals Interaction between Embryo Morphology and Toll Signaling Pathway during Evolution
journal, August 2014
- Ambrosi, Priscilla; Chahda, Juan Sebastian; Koslen, Hannah R.
- PLoS Computational Biology, Vol. 10, Issue 8
Spatially varying cis-regulatory divergence in Drosophila embryos elucidates cis-regulatory logic
journal, November 2018
- Combs, Peter A.; Fraser, Hunter B.
- PLOS Genetics, Vol. 14, Issue 11
Depleting Gene Activities in Early Drosophila Embryos with the “Maternal-Gal4–shRNA” System
journal, January 2013
- Staller, Max V.; Yan, Dong; Randklev, Sakara
- Genetics, Vol. 193, Issue 1
High-resolution gene expression data from blastoderm embryos of the scuttle fly Megaselia abdita
journal, March 2015
- Wotton, Karl R.; Jiménez-Guri, Eva; Crombach, Anton
- Scientific Data, Vol. 2, Issue 1
Quantitative Comparison of the Anterior-Posterior Patterning System in the Embryos of Five Drosophila Species
journal, July 2019
- Wunderlich, Zeba; Fowlkes, Charless C.; Eckenrode, Kelly B.
- G3 Genes|Genomes|Genetics, Vol. 9, Issue 7
Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity
journal, January 2018
- Park, Jeehae; Estrada, Javier; Johnson, Gemma
- eLife
Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity
journal, June 2019
- Park, Jeehae; Estrada, Javier; Johnson, Gemma
- eLife, Vol. 8
Reply to Jiang and Zhang: Parallel transcriptomic signature of monogamy: What is the null hypothesis anyway?
journal, August 2019
- Young, Rebecca L.; Hofmann, Hans A.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 36
WholeCellViz: data visualization for whole-cell models
journal, January 2013
- Lee, Ruby; Karr, Jonathan R.; Covert, Markus W.
- BMC Bioinformatics, Vol. 14, Issue 1
Spatially varying cis-regulatory divergence in Drosophila embryos elucidates cis-regulatory logic
posted_content, November 2017
- Combs, Peter A.; Fraser, Hunter B.
- PLOS Genetics
Towards 3D in silico modeling of the sea urchin embryonic development
journal, September 2013
- Rizzi, Barbara; Peyrieras, Nadine
- Journal of Chemical Biology, Vol. 7, Issue 1
Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers
journal, March 2016
- Wunderlich, Zeba; Bragdon, Meghan D. J.; Vincent, Ben J.
- Cell Reports, Vol. 14, Issue 12
High-resolution gene expression data from blastoderm embryos of the scuttle fly Megaselia abdita
journal, March 2015
- Wotton, Karl R.; Jiménez-Guri, Eva; Crombach, Anton
- Scientific Data, Vol. 2, Issue 1
Shaped Singular Spectrum Analysis for Quantifying Gene Expression, with Application to the EarlyDrosophilaEmbryo
journal, January 2015
- Shlemov, Alex; Golyandina, Nina; Holloway, David
- BioMed Research International, Vol. 2015
WholeCellViz: data visualization for whole-cell models
journal, January 2013
- Lee, Ruby; Karr, Jonathan R.; Covert, Markus W.
- BMC Bioinformatics, Vol. 14, Issue 1
A novel procedure for absolute real-time quantification of gene expression patterns
journal, January 2012
- Lu, Yingqing; Xie, Lulu; Chen, Jiani
- Plant Methods, Vol. 8, Issue 1
A Digital Framework to Build, Visualize and Analyze a Gene Expression Atlas with Cellular Resolution in Zebrafish Early Embryogenesis
journal, June 2014
- Castro-González, Carlos; Luengo-Oroz, Miguel A.; Duloquin, Louise
- PLoS Computational Biology, Vol. 10, Issue 6
Modeling of the Dorsal Gradient across Species Reveals Interaction between Embryo Morphology and Toll Signaling Pathway during Evolution
journal, August 2014
- Ambrosi, Priscilla; Chahda, Juan Sebastian; Koslen, Hannah R.
- PLoS Computational Biology, Vol. 10, Issue 8
Allele-specific expression elucidates cis-regulatory logic
journal, November 2018
- Delbare, Sofie Y. N.; Clark, Andrew G.
- PLOS Genetics, Vol. 14, Issue 11
Extensive divergence of transcription factor binding in Drosophila embryos with highly conserved gene expression
text, January 2013
- Paris, Mathilde; Kaplan, Tommy; Li, Xiao Yong
- arXiv
Dissecting the sharp response of a canonical developmental enhancer reveals multiple sources of cooperativity
journal, June 2019
- Park, Jeehae; Estrada, Javier; Johnson, Gemma
- eLife, Vol. 8