Dynamic Patterning by Morphogens Illuminated by Cis-regulatory Studies

Overview

Journal Development

Specialty Biology

Date 2021 Jan 21

PMID 33472851

Citations 7

Authors

Jihyun Irizarry

Angelike Stathopoulos

Affiliations

Soon will be listed here.

Abstract

Morphogen concentration changes in space as well as over time during development. However, how these dynamics are interpreted by cells to specify fate is not well understood. Here, we focus on two morphogens: the maternal transcription factors Bicoid and Dorsal, which directly regulate target genes to pattern embryos. The actions of these factors at enhancers has been thoroughly dissected and provides a rich platform for understanding direct input by morphogens and their changing roles over time. Importantly, Bicoid and Dorsal do not work alone; we also discuss additional inputs that work with morphogens to control spatiotemporal gene expression in embryos.

Citing Articles

Target gene responses differ when transcription factor levels are acutely decreased by nuclear export versus degradation.

McGehee J, Stathopoulos A Development. 2024; 151(21).

PMID: 39397716 PMC: 11574349. DOI: 10.1242/dev.202775.

Target gene responses differ when transcription factor levels are acutely decreased by nuclear export versus degradation.

McGehee J, Stathopoulos A bioRxiv. 2024; .

PMID: 38826476 PMC: 11142056. DOI: 10.1101/2024.05.20.595009.

Revisiting bicoid function: complete inactivation reveals an additional fundamental role in Drosophila egg geometry specification.

Baumgartner S Hereditas. 2024; 161(1):1.

PMID: 38167241 PMC: 10759373. DOI: 10.1186/s41065-023-00305-9.

Setting the stage for development: the maternal-to-zygotic transition in Drosophila.

Harrison M, Marsh A, Rushlow C Genetics. 2023; 225(2).

PMID: 37616526 PMC: 10550319. DOI: 10.1093/genetics/iyad142.

Chromatin accessibility in the Drosophila embryo is determined by transcription factor pioneering and enhancer activation.

Brennan K, Weilert M, Krueger S, Pampari A, Liu H, Yang A Dev Cell. 2023; 58(19):1898-1916.e9.

PMID: 37557175 PMC: 10592203. DOI: 10.1016/j.devcel.2023.07.007.

References

Schulz K, Bondra E, Moshe A, Villalta J, Lieb J, Kaplan T . Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo. Genome Res. 2015; 25(11):1715-26. PMC: 4617967. DOI: 10.1101/gr.192682.115. View

Chahda J, Sousa-Neves R, Mizutani C . Variation in the dorsal gradient distribution is a source for modified scaling of germ layers in Drosophila. Curr Biol. 2013; 23(8):710-6. PMC: 3731453. DOI: 10.1016/j.cub.2013.03.031. View

Ten Bosch J, Benavides J, Cline T . The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development. 2006; 133(10):1967-77. DOI: 10.1242/dev.02373. View

Wu H, Manu , Jiao R, Ma J . Temporal and spatial dynamics of scaling-specific features of a gene regulatory network in Drosophila. Nat Commun. 2015; 6:10031. PMC: 4686680. DOI: 10.1038/ncomms10031. View

Huang A, Saunders T . A matter of time: Formation and interpretation of the Bicoid morphogen gradient. Curr Top Dev Biol. 2020; 137:79-117. DOI: 10.1016/bs.ctdb.2019.11.016. View

Boija A, Mannervik M . Initiation of diverse epigenetic states during nuclear programming of the Drosophila body plan. Proc Natl Acad Sci U S A. 2016; 113(31):8735-40. PMC: 4978291. DOI: 10.1073/pnas.1516450113. View

Bollenbach T, Pantazis P, Kicheva A, Bokel C, Gonzalez-Gaitan M, Julicher F . Precision of the Dpp gradient. Development. 2008; 135(6):1137-46. DOI: 10.1242/dev.012062. View

Koromila T, Gao F, Iwasaki Y, He P, Pachter L, Gergen J . Odd-paired is a pioneer-like factor that coordinates with Zelda to control gene expression in embryos. Elife. 2020; 9. PMC: 7417190. DOI: 10.7554/eLife.59610. View

Katikala L, Aihara H, Passamaneck Y, Gazdoiu S, Jose-Edwards D, Kugler J . Functional Brachyury binding sites establish a temporal read-out of gene expression in the Ciona notochord. PLoS Biol. 2013; 11(10):e1001697. PMC: 3812116. DOI: 10.1371/journal.pbio.1001697. View

10.

Mir M, Stadler M, Ortiz S, Hannon C, Harrison M, Darzacq X . Dynamic multifactor hubs interact transiently with sites of active transcription in embryos. Elife. 2018; 7. PMC: 6307861. DOI: 10.7554/eLife.40497. View

11.

Hong J, Hendrix D, Papatsenko D, Levine M . How the Dorsal gradient works: insights from postgenome technologies. Proc Natl Acad Sci U S A. 2008; 105(51):20072-6. PMC: 2629255. DOI: 10.1073/pnas.0806476105. View

12.

Liu J, Ma J . Uncovering a dynamic feature of the transcriptional regulatory network for anterior-posterior patterning in the Drosophila embryo. PLoS One. 2013; 8(4):e62641. PMC: 3639989. DOI: 10.1371/journal.pone.0062641. View

13.

Briscoe J, Chen Y, Jessell T, Struhl G . A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol Cell. 2001; 7(6):1279-91. DOI: 10.1016/s1097-2765(01)00271-4. View

14.

Garcia M, Nahmad M, Reeves G, Stathopoulos A . Size-dependent regulation of dorsal-ventral patterning in the early Drosophila embryo. Dev Biol. 2013; 381(1):286-99. PMC: 3968923. DOI: 10.1016/j.ydbio.2013.06.020. View

15.

Ochoa-Espinosa A, Yu D, Tsirigos A, Struffi P, Small S . Anterior-posterior positional information in the absence of a strong Bicoid gradient. Proc Natl Acad Sci U S A. 2009; 106(10):3823-8. PMC: 2656164. DOI: 10.1073/pnas.0807878105. View

16.

Datta R, Ling J, Kurland J, Ren X, Xu Z, Yucel G . A feed-forward relay integrates the regulatory activities of Bicoid and Orthodenticle via sequential binding to suboptimal sites. Genes Dev. 2018; 32(9-10):723-736. PMC: 6004077. DOI: 10.1101/gad.311985.118. View

17.

Bothma J, Magliocco J, Levine M . The snail repressor inhibits release, not elongation, of paused Pol II in the Drosophila embryo. Curr Biol. 2011; 21(18):1571-7. PMC: 3186076. DOI: 10.1016/j.cub.2011.08.019. View

18.

Zeitlinger J, Zinzen R, Stark A, Kellis M, Zhang H, Young R . Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 2007; 21(4):385-90. PMC: 1804326. DOI: 10.1101/gad.1509607. View

19.

Manu , Surkova S, Spirov A, Gursky V, Janssens H, Kim A . Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLoS Comput Biol. 2009; 5(3):e1000303. PMC: 2646127. DOI: 10.1371/journal.pcbi.1000303. View

20.

Reeves G, Trisnadi N, Truong T, Nahmad M, Katz S, Stathopoulos A . Dorsal-ventral gene expression in the Drosophila embryo reflects the dynamics and precision of the dorsal nuclear gradient. Dev Cell. 2012; 22(3):544-57. PMC: 3469262. DOI: 10.1016/j.devcel.2011.12.007. View