Abstract
Bicoid (Bcd) protein distributes in a concentration gradient that organizes the anterior/posterior axis of the Drosophila embryo. It has been understood that bcd RNA is sequestered at the anterior pole during oogenesis, is not translated until fertilization, and produces a protein gradient that functions in the syncytial blastoderm after 9-10 nuclear divisions. However, technical issues limited the sensitivity of analysis of pre-syncytial blastoderm embryos and precluded studies of oocytes after stage 13. We developed methods to analyze stage 14 oocytes and pre-syncytial blastoderm embryos, and found that stage 14 oocytes make Bcd protein, that bcd RNA and Bcd protein distribute in matching concentration gradients in the interior of nuclear cycle 2-6 embryos, and that Bcd regulation of target gene expression is apparent at nuclear cycle 7, two cycles prior to syncytial blastoderm. We discuss the implications for the generation and function of the Bcd gradient.
Highlights
The discovery of the concentration gradient of Bicoid (Bcd) protein in the early Drosophila embryo established the existence and functional importance of a morphogen gradient for the first time (Driever and Nusslein-Volhard, 1988a, 1988b; Frigerio et al, 1986); it was a watershed moment in developmental biology
Whether the protein gradient forms by passive diffusion following synthesis of Bcd protein at more anterior locations (Gregor et al, 2007; Little et al, 2011), or is produced in place by the bcd mRNA concentration gradient is in dispute (Fahmy et al, 2014; Spirov et al, 2009)
By using sensitive methods that we modified for studies of the early embryo, we found that the processes that generate the Bcd protein gradient are more complex and operate earlier than had been appreciated, and that the function of the Bcd gradient begins prior to formation of the syncytial blastoderm
Summary
The discovery of the concentration gradient of Bicoid (Bcd) protein in the early Drosophila embryo established the existence and functional importance of a morphogen gradient for the first time (Driever and Nusslein-Volhard, 1988a, 1988b; Frigerio et al, 1986); it was a watershed moment in developmental biology These and subsequent studies showed that Bcd protein is present at the cortex of pre-cellular, syncytial blastoderm embryos, with levels that are highest at the anterior end and that decline exponentially toward the posterior (Driever and Nusslein-Volhard, 1988b; Gregor et al, 2007; Spirov et al, 2009). Various measures, including in situ hybridization (Erickson and Cline, 1993; Pritchard and Schubiger, 1996), RT-PCR (Harrison et al, 2010), genome array hybridization (De Renzis et al, 2007; Little et al, 2011; Lu et al, 2009), RNA seq (Lott et al, 2011), DNA footprinting (Harrison et al, 2010), chromatin profiling (Harrison et al, 2011) and ChIP-seq (Blythe and Wieschaus, 2015), show that the zygotic genome is transcriptionally activated during the syncytial blastoderm period
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