The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA.
The Bicoid morphogen gradient directs the patterning of cell fates along the anterior-posterior axis of the syncytial Drosophila embryo and serves as a paradigm of morphogen-mediated patterning. The simplest models of gradient formation rely on constant protein synthesis and diffusion from anteriorl...
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Public Library of Science (PLoS)
2011-03-01
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| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000596&type=printable |
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| author | Shawn C Little Gašper Tkačik Thomas B Kneeland Eric F Wieschaus Thomas Gregor |
| author_facet | Shawn C Little Gašper Tkačik Thomas B Kneeland Eric F Wieschaus Thomas Gregor |
| author_sort | Shawn C Little |
| collection | DOAJ |
| description | The Bicoid morphogen gradient directs the patterning of cell fates along the anterior-posterior axis of the syncytial Drosophila embryo and serves as a paradigm of morphogen-mediated patterning. The simplest models of gradient formation rely on constant protein synthesis and diffusion from anteriorly localized source mRNA, coupled with uniform protein degradation. However, currently such models cannot account for all known gradient characteristics. Recent work has proposed that bicoid mRNA spatial distribution is sufficient to produce the observed protein gradient, minimizing the role of protein transport. Here, we adapt a novel method of fluorescent in situ hybridization to quantify the global spatio-temporal dynamics of bicoid mRNA particles. We determine that >90% of all bicoid mRNA is continuously present within the anterior 20% of the embryo. bicoid mRNA distribution along the body axis remains nearly unchanged despite dynamic mRNA translocation from the embryo core to the cortex. To evaluate the impact of mRNA distribution on protein gradient dynamics, we provide detailed quantitative measurements of nuclear Bicoid levels during the formation of the protein gradient. We find that gradient establishment begins 45 minutes after fertilization and that the gradient requires about 50 minutes to reach peak levels. In numerical simulations of gradient formation, we find that incorporating the actual bicoid mRNA distribution yields a closer prediction of the observed protein dynamics compared to modeling protein production from a point source at the anterior pole. We conclude that the spatial distribution of bicoid mRNA contributes to, but cannot account for, protein gradient formation, and therefore that protein movement, either active or passive, is required for gradient formation. |
| format | Article |
| id | doaj-art-88d21b9df7364cb2b41c0b3f1e3fe70b |
| institution | OA Journals |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2011-03-01 |
| publisher | Public Library of Science (PLoS) |
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| spelling | doaj-art-88d21b9df7364cb2b41c0b3f1e3fe70b2025-08-20T02:34:06ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852011-03-0193e100059610.1371/journal.pbio.1000596The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA.Shawn C LittleGašper TkačikThomas B KneelandEric F WieschausThomas GregorThe Bicoid morphogen gradient directs the patterning of cell fates along the anterior-posterior axis of the syncytial Drosophila embryo and serves as a paradigm of morphogen-mediated patterning. The simplest models of gradient formation rely on constant protein synthesis and diffusion from anteriorly localized source mRNA, coupled with uniform protein degradation. However, currently such models cannot account for all known gradient characteristics. Recent work has proposed that bicoid mRNA spatial distribution is sufficient to produce the observed protein gradient, minimizing the role of protein transport. Here, we adapt a novel method of fluorescent in situ hybridization to quantify the global spatio-temporal dynamics of bicoid mRNA particles. We determine that >90% of all bicoid mRNA is continuously present within the anterior 20% of the embryo. bicoid mRNA distribution along the body axis remains nearly unchanged despite dynamic mRNA translocation from the embryo core to the cortex. To evaluate the impact of mRNA distribution on protein gradient dynamics, we provide detailed quantitative measurements of nuclear Bicoid levels during the formation of the protein gradient. We find that gradient establishment begins 45 minutes after fertilization and that the gradient requires about 50 minutes to reach peak levels. In numerical simulations of gradient formation, we find that incorporating the actual bicoid mRNA distribution yields a closer prediction of the observed protein dynamics compared to modeling protein production from a point source at the anterior pole. We conclude that the spatial distribution of bicoid mRNA contributes to, but cannot account for, protein gradient formation, and therefore that protein movement, either active or passive, is required for gradient formation.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000596&type=printable |
| spellingShingle | Shawn C Little Gašper Tkačik Thomas B Kneeland Eric F Wieschaus Thomas Gregor The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. PLoS Biology |
| title | The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. |
| title_full | The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. |
| title_fullStr | The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. |
| title_full_unstemmed | The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. |
| title_short | The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. |
| title_sort | formation of the bicoid morphogen gradient requires protein movement from anteriorly localized mrna |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1000596&type=printable |
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