Molecular Biology of the Cell by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morgan, Martin Raff, Keith Roberts, Peter Walter by by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morg

1158 Chapter 21: Development of Multicellular Organisms
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 transcription
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.
(A) Bicoid mRNA
(B) Bicoid protein
Bicoid protein
anterior
(C)
wild type
Bicoid mutant
posterior
Figure 21–16 The Bicoid protein
gradient. (A) Bicoid mRNA is deposited at
the anterior pole during oogenesis.
(B) Local MBoC6 translation n22.208/22.17 followed by diffusion
generates the Bicoid protein gradient.
(C) Absence of the Bicoid protein gradient
in embryos from Bicoid homozygous
mutant mothers. (A and B, courtesy of
Stephen Small.)
POSTERIOR SYSTEM
ANTERIOR SYSTEM
TERMINAL SYSTEM
DORSOVENTRAL SYSTEM
localized mRNA (Nanos )
localized mRNA (Bicoid )
transmembrane receptors (Torso)
transmembrane receptors (Toll)
DETERMINING
• germ cells vs. somatic cells
• head vs. rear
• body segments
DETERMINING
• ectoderm vs. mesoderm vs. endoderm
• terminal structures
Figure 21–17 The organization of the four egg-polarity gradient systems in Drosophila. Nanos is a translational repressor that governs the
formation of the abdomen. Localized Nanos mRNA is also incorporated into the germ cells as they form at the posterior of the embryo, and Nanos
protein is necessary for germ-line development. Bicoid protein is a transcriptional activator that determines the head and thoracic regions. Toll and
Torso are receptor proteins that are distributed all over the membrane but are activated only at the sites indicated by the coloring, through localized
exposure to the extracellular ligands Spaetzle (the ligand for Toll) and Trunk (the ligand for Torso). Toll activity determines the mesoderm and Torso
activity determines the formation of terminal structures.