Journal Article

Bicoid gradient formation and function in the Drosophila pre-syncytial blastoderm

Ali-Murthy, Zehra, Kornberg, Thomas B

2016

Overview

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. As an embryo develops, a single cell transforms into a collection of different types of cells. One protein that is crucial for this process in fruit fly embryos is Bicoid. Thirty years ago, scientists discovered that Bicoid protein is concentrated at the head end of the embryo and gradually decreases in amount towards the rear end. This concentration gradient of Bicoid protein organizes the embryo body and regulates the expression of many genes, thus directing the cells to develop different identities. Several assumptions had been made about how this gradient is established. It was thought that in the unfertilized egg, the mRNA molecules that will be translated to produce Bicoid proteins are stored in an inactive state in the region of the egg that later develops into the embryo’s head. In the embryo, the mRNA molecules were believed to remain in the head region while being translated, with the newly formed proteins then gradually spreading from this site to create the Bicoid gradient. It was also thought that no Bicoid proteins are stored in the unfertilized egg. However, no known methods were sensitive enough to investigate these assumptions. Now, using newer and more sensitive methods, Ali-Murthy and Kornberg show that Bicoid protein is present in the unfertilized fruit fly egg in the same region as the mRNA molecules that make Bicoid. Furthermore, the Bicoid gradient forms when the embryo has fewer than 32 nuclei, much earlier in development than previously thought. The Bicoid protein also does not appear to spread passively towards the rear of the embryo, but is transported in a more orchestrated manner. Overall, Ali-Murthy and Kornberg’s results suggest that the early fruit fly embryo is more organized and actively regulated than had been previously understood. This paves the way for further studies that use sensitive techniques to investigate this early stage of development.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Bcd protein / bicoid / Blastoderm / Blastoderm - chemistry / Blastoderm - physiology / Blastula / Developmental Biology and Stem Cells / Drosophila / Drosophila - embryology / embryo / Embryos / Fertilization / Gene expression / Gene Expression Regulation / Genomes / Homeodomain Proteins - analysis / Homeodomain Proteins - metabolism / Hybridization / Insects / Krüppel / oocyte / Oocytes / Oogenesis / Physiological aspects / Proteins / Ribonucleic acid / RNA / RNA, Messenger - analysis / Trans-Activators - analysis / Trans-Activators - metabolism