Abstract
Embryogenesis relies on instructions provided by spatially organized signaling molecules known as morphogens. Understanding the principles behind morphogen distribution and how cells interpret locally this information remains a major challenge in developmental biology. Here, we introduce morphogen‐age measurements as a novel approach to test models of morphogen gradient formation. Using a tandem fluorescent timer as a protein age sensor, we find a gradient of increasing age of Bicoid along the anterior–posterior axis in the early Drosophila embryo. Quantitative analysis of the protein age distribution across the embryo reveals that the synthesis–diffusion–degradation model is the most likely model underlying Bicoid gradient formation, and rules out other hypotheses for gradient formation. Moreover, we show that the timer can detect transitions in the dynamics associated with syncytial cellularization. Our results provide new insight into Bicoid gradient formation and demonstrate how morphogen‐age information can complement knowledge about movement, abundance, and distribution, which should be widely applicable to other systems.
Highlights
Acquisition of different cell fates at specific spatial and temporal locations is an essential process driving development
The classic view of Bcd gradient formation is that the protein is synthesized in the anterior pole of the Drosophila blastoderm and forms a long range gradient through diffusion, with the gradient shape adapted by protein degradation (SDD model) (Driever & Nusslein-Volhard, 1988a,b; Gregor et al, 2007b)
Two types of models have been considered for Bcd gradient formation: localized Bcd synthesis in the anterior with subsequent long-ranged transport; and pre-patterned synthesis and restricted protein transport, more complicated scenarios, such as spatially patterned degradation, are imaginable
Summary
Acquisition of different cell fates at specific spatial and temporal locations is an essential process driving development. The classic view of Bcd gradient formation is that the protein is synthesized in the anterior pole of the Drosophila blastoderm and forms a long range gradient through diffusion, with the gradient shape adapted by protein degradation (SDD model) (Driever & Nusslein-Volhard, 1988a,b; Gregor et al, 2007b). Such a model agrees well with the observed Bcd gradient in embryos undergoing cellularization, where Bcd levels decay exponentially toward the posterior pole (Houchmandzadeh et al, 2002; Gregor et al, 2007b). Several other models involving alternative mechanisms for Bcd production and distribution have been proposed, all of which are capable of producing an exponential-like concentration profile, as further outlined below (Coppey et al, 2007; Hecht et al, 2009; Spirov et al, 2009; Dilao & Muraro, 2010; Grimm et al, 2010; Kavousanakis et al, 2010)
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