Homologous tails?
Or tales of homology?
James D. McGhee
Summary
Classical mutations at the mouse
Brachyury
(
T
) locus
were discovered because they lead to shortened tails in
heterozygous newborns.
no tail
(
ntl
) mutants in the
zebrafish, as their name suggests, show a similar
phenotype. In
Drosophila
, mutants in the
brachyenteron
(
byn
) gene disrupt hindgut formation. These genes all
encode T-box proteins, a class of sequence-specific
DNA binding proteins and transcription factors. Muta-
tions in the
C. elegans mab-9
gene cause massive
defects in the male tail because of failed fate decisions
in two tail progenitor cells. In a recent paper, Woollard
and Hodgkin
(1)
have cloned the
mab-9
gene and found
that it too encodes a T-box protein, similar to
Brachyury
in vertebrates and
brachyenteron
in
Drosophila
. The
authors suggest that their results support models for an
evolutionarily ancient role for these genes in hindgut
formation. We will discuss this proposal and try to
decide whether the gene sequences, gene interactions
and gene expression patterns allow any conclusions to
be made about the rear end of the ancestral meta-
zoan. BioEssays 22:781±785, 2000.
ß 2000 John Wiley & Sons, Inc.
Introduction
During the past two decades, with the increasingly detailed
analyses of developmental genetics in diverse animals and
the explosion of information about genomic sequences, the
fundamental unity of metazoan organisms has become
apparent. Metazoans (more particularly, triploblastic metazo-
ans) appear to be monophyletic, descended from some
archetype that first appeared 500±1000 million years ago.
(2,3)
Striking examples of conserved regulatory molecules are
brought out to support such a model. First and foremost are
the genes of the hox clusters with their conserved sequences,
chromosomal arrangement, spatial distribution of expression
patterns and apparent role in regional specification along the
anterior-posterior axis of all metazoans (see references in
Ref. 3). A second example is the Pax6 genes that are
involved in eye development.
(3)
In addition, there are the
vertebrate Brachyury genes which are crucial for normal
development
(4±8)
and seem to provide a further example of
widely conserved transcriptional regulators. Nonetheless, as
will be discussed below, these latter genes do not seem to fit
easily into the troika of conserved gene sequences, con-
served regulatory pathways and conserved expression
domains. Before considering why this may be so, we will first
describe the principal result of a recent paper by Woollard and
Hodgkin
(1)
because it reveals the first biological function
of a Brachyury-like gene in the nematode Caenorhabditis
elegans.
Sexual dimorphism in
Caenorhabditis elegans
Because of its defined cell lineage, excellent genetics and
complete genomic sequence, the small worm Caenorhabditis
elegans (C. elegans) has become a popular and powerful
experimental organism for the study of most aspects of
metazoan biology.
(9,10)
Worms normally propagate as self-
fertilizing hermaphrodites but occasional males arise be-
cause of X-chromosome nondisjunction. Males differ from
hermaphrodites both in behaviour and morphology, particu-
larly in the region of the tail
(11)
(see Fig. 1). Externally, the
male tail displays a fanlike sensory arrangement that allows
location of the hermaphrodite vulva. Internally, a proctodeum
joins the male intestine and vas deferens to the exterior, and
contains a pair of copulatory spicules with associated nerves
and muscles. As depicted in Fig. 1, proliferation of four post-
embryonic blast cells (F, U, Y and especially B) produce
much of the internal structure of the male tail by the discrete
stereotyped cell lineages typical of C. elegans.
The
mab-9
gene governs cell fate switches in
the male tail
The Hodgkin lab has had a long standing interest in C.
elegans sex determination, from the original definition of the
genetic pathway,
(12)
through the mechanism of chromosome
counting required for the correct male vs. hermaphrodite
decision
(13)
and now to the molecular basis of sexual
dimorphisms.
(1)
The mab-9 gene (where mab stands for
male abnormal) was identified as a mutation that reduces the
male tail to a gnarled stump.
(14)
At the cellular level, the mab-
9 defects can be ascribed to fate changes that are not
made,
(15)
a relatively common cause of developmental
derangements in C. elegans. In this case, the two posterior
blast cells F and B (see Fig. 1) mistakenly adopt the fate of
their anterior counterparts U and Y, leading to massive
defects in the proctodeum and spicules. Similar mistaken cell
BioEssays 22:781±785, ß 2000 John Wiley & Sons, Inc. BioEssays 22.9 781
Department of Biochemistry and Molecular Biology, Genes and
Development Research Group, University of Calgary, Calgary,
Alberta, Canada. T2N 4N1. E-mail: jmcghee@ucalgary.ca
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