Dataset Information

Probing intrinsic properties of a robust morphogen gradient in Drosophila.

ABSTRACT: A remarkable feature of development is its reproducibility, the ability to correct embryo-to-embryo variations and instruct precise patterning. In Drosophila, embryonic patterning along the anterior-posterior axis is controlled by the morphogen gradient Bicoid (Bcd). In this article, we describe quantitative studies of the native Bcd gradient and its target Hunchback (Hb). We show that the native Bcd gradient is highly reproducible and is itself scaled with embryo length. While a precise Bcd gradient is necessary for precise Hb expression, it still has positional errors greater than Hb expression. We describe analyses further probing mechanisms for Bcd gradient scaling and correction of its residual positional errors. Our results suggest a simple model of a robust Bcd gradient sufficient to achieve scaled and precise activation of its targets. The robustness of this gradient is conferred by its intrinsic properties of "self-correcting" the inevitable input variations to achieve a precise and reproducible output.

SUBMITTER: He F

PROVIDER: S-EPMC2629455 | biostudies-literature | 2008 Oct

REPOSITORIES: biostudies-literature

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Probing intrinsic properties of a robust morphogen gradient in Drosophila.

He Feng F Wen Ying Y Deng Jingyuan J Lin Xiaodong X Lu Long Jason LJ Jiao Renjie R Ma Jun J

Developmental cell 20081001 4

A remarkable feature of development is its reproducibility, the ability to correct embryo-to-embryo variations and instruct precise patterning. In Drosophila, embryonic patterning along the anterior-posterior axis is controlled by the morphogen gradient Bicoid (Bcd). In this article, we describe quantitative studies of the native Bcd gradient and its target Hunchback (Hb). We show that the native Bcd gradient is highly reproducible and is itself scaled with embryo length. While a precise Bcd gra ...[more]

PMID: 18854140

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Project description:In multicellular organisms, the timing and placement of gene expression in a developing tissue assigns the fate of each cell in the embryo in order for a uniform field of cells to differentiate into a reproducible pattern of organs and tissues. This positional information is often achieved through the action of spatial gradients of morphogens. Spatial patterns of gene expression are paradoxically robust to variations in morphogen dosage, given that, by definition, gene expression must be sensitive to morphogen concentration. In this work we investigate the robustness of the Dorsal/NF-κB signaling module with respect to perturbations to the dosage of maternally-expressed dorsal mRNA. The Dorsal morphogen gradient patterns the dorsal-ventral axis of the early Drosophila embryo, and we found that an empirical description of the Dorsal gradient is highly sensitive to maternal dorsal dosage. In contrast, we found experimentally that gene expression patterns are highly robust. Although the components of this signaling module have been characterized in detail, how their function is integrated to produce robust gene expression patterns to variations in the dorsal maternal dosage is still unclear. Therefore, we analyzed a mechanistic model of the Dorsal signaling module and found that Cactus, a cytoplasmic inhibitor for Dorsal, must be present in the nucleus for the system to be robust. Furthermore, active Toll, the receptor that dissociates Cactus from Dorsal, must be saturated. Finally, the vast majority of robust descriptions of the system require facilitated diffusion of Dorsal by Cactus. Each of these three recently-discovered mechanisms of the Dorsal module are critical for robustness. These mechanisms synergistically contribute to changing the amplitude and shape of the active Dorsal gradient, which is required for robust gene expression. Our work highlights the need for quantitative understanding of biophysical mechanisms of morphogen gradients in order to understand emergent phenotypes, such as robustness.

Dataset Information

Probing intrinsic properties of a robust morphogen gradient in Drosophila.

Publications

Probing intrinsic properties of a robust morphogen gradient in Drosophila.

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