Abstract
The Bicoid (Bcd) protein gradient in Drosophila serves as a paradigm for gradient formation in textbooks. To explain the generation of the gradient, the ARTS model, which is based on the observation of a bcd mRNA gradient, proposes that the bcd mRNA, localized at the anterior pole at fertilization, migrates along microtubules (MTs) at the cortex to the posterior to form a bcd mRNA gradient which is translated to form a protein gradient. To fulfil the criteria of the ARTS model, an early cortical MT network is thus a prerequisite. We report hitherto undiscovered MT activities in the early embryo important for bcd mRNA transport: (i) an early and omnidirectional MT network exclusively at the anterior cortex of early nuclear cycle embryos showing activity during metaphase and anaphase only, (ii) long MTs up to 50 µm extending into the yolk at blastoderm stage to enable basal-apical transport. The cortical MT network is not anchored to the actin cytoskeleton. The posterior transport of the mRNA via the cortical MT network critically depends on maternally-expressed αTubulin67C and the minus-end motor Ncd. In either mutant, cortical transport of the bcd mRNA does not take place and the mRNA migrates along another yet undisclosed interior MT network, instead. Our data strongly corroborate the ARTS model and explain the occurrence of the bcd mRNA gradient.
Highlights
The Bicoid (Bcd) protein is a paradigm for morphogen gradient formation taught in textbooks and studied for more than two decades
In the large blowfly Lucilia sericata, the gradient appears very similar (Fig. S1C, D), suggesting that the mRNA gradient as well as the ARTS model are universal among Diptera
Note the short MT threads at the cortex. (C) a kavarnull/Df(3L)55 embryo, stained for the bcd mRNA along with DAPI to reveal the nucleus. (D) stage 10 and (E) stage 14 aTub67C3/aTub67C3 oocytes stained for bcd mRNA and DAPI
Summary
The Bicoid (Bcd) protein is a paradigm for morphogen gradient formation taught in textbooks and studied for more than two decades. The ARTS (Active RNA Transport and Synthesis) model proposes that the bcd mRNA is actively transported along the cortex in a posterior direction from its anterior pole to form an mRNA gradient which serves as template for the synthesis of Bcd. Recently, the SDD model encountered some severe difficulties: the diffusion coefficient of Bcd was found to be two orders of magnitude too low to establish a steady-state Bcd gradient by the blastoderm stage [5]. Important to note: the ARTS model does not argue against a high diffusion coefficient of Bcd, it is only largely irrelevant for the model
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