egg-polarity Genes encode Macromolecules Deposited in the egg to Organize the axes of the early Drosophila embryo
As in most insects, the main axes of the future body of Drosophila are defined before fertilization by a complex exchange of signals between the developing egg,
Figure 21–15 Development of the Drosophila egg from fertilization to the cellular blastoderm stage.
or oocyte, and the follicle cells that surround it in the ovary. In the stages before fertilization, the anteroposterior and dorsoventral axes of the future embryo become defined by four systems of egg-polarity genes that create landmarks— either mRNA or protein—in the developing oocyte. Following fertilization, each landmark serves as a beacon, providing a signal that organizes the developmental process in its neighborhood.
The nature of the genes emerged from studies of mutants in which the patterning of the embryo was altered. One class of mutations gave embryos with disrupted polarity—for example, tail-end structures at both ends of the body, with no head-end structures. This class of mutations identified the set of egg-polarity genes. The egg-polarity gene responsible for the signal that organizes the anterior end of the embryo is called Bicoid. A deposit of Bicoid mRNA molecules is localized, before fertilization, at the anterior end of the egg. Upon fertilization, the mRNA is translated to produce Bicoid protein. This protein is an intracellular morphogen and transcription regulator that diffuses away from its source to form a concentration gradient within the syncytial cytoplasm, with its maximum at the head end of the embryo (Figure 21–16). The different concentrations of Bicoid along the A-P axis help determine different cell fates by regulating the transcrip tion of genes in the nuclei of the syncytial blastoderm (discussed in Chapter 7).
Of the three other egg-polarity gene systems, two contribute to patterning the syncytial nuclei along the A-P axis and one to patterning them along the D-V axis. Together with the Bicoid group of genes, and acting in a broadly similar way, their gene products mark out three fundamental partitions of body regions—head versus rear, dorsal versus ventral, and endoderm versus mesoderm and ectoderm— as well as a fourth partition, no less fundamental to the body plan of animals: the distinction between germ cells and somatic cells (Figure 21–17).
The egg-polarity genes have a further special feature: they are all maternal-effect genes, in that it is the mother’s genome rather than the zygote’s genome that is critical. For example, a fly whose chromosomes are mutant in both copies of the Bicoid gene but who is born from a mother carrying one normal copy of Bicoid develops perfectly normally, without any defects in the head pattern. However, if that offspring is a female, she cannot deposit any functional Bicoid mRNA into her own eggs, which will therefore develop into headless embryos, regardless of the father’s genotype.
The egg-polarity genes act first in a hierarchy of gene systems that define a progressively more detailed pattern of body parts. In the next few pages, we begin with the molecular mechanisms that pattern the developing Drosophila embryo and larva along the A-P axis, before considering the patterning along the D-V axis.
Figure 21–16 The Bicoid protein gradient. (a) Bicoid mrNa is deposited at the anterior pole during oogenesis.
Local translation followed by diffusion generates the Bicoid protein gradient.
absence of the Bicoid protein gradient in embryos from Bicoid homozygous mutant mothers. (a and B, courtesy of Stephen Small.)