Development 102, 223-235 (1988)
Printed in Great Britain © The Company of Biologists Limited 1988
223
Development of the two-part pattern during regeneration of the head in
hydra
P. M. BODE
1
, T. A. AWAD
1
, O. KOIZUMI
2
, Y. NAKASHIMA
2
, C. J. P. GRIMMELIKHUIJZEN
3
and
H. R. BODE
1
'Developmental Biology Center, Department of Developmental and Cell Biology, University of California at Irvine, Irvine, CA 92717, USA
2
Physiological Laboratory, Department of Science, Fukuoka Women's University, Fukuoka, Japan
^Zoological Institute, University of Heidelberg, Heidelberg, FRG
Summary
The head of a hydra is composed of two parts, a domed
hypostome with a mouth at the top and a ring of
tentacles below. When animals are decapitated a new
head regenerates. During the process of regeneration
the apical tip passes through a transient stage in which
it exhibits tentacle-like characteristics before becom-
ing a hypostome. This was determined from markers
which appeared before morphogenesis took place.
The first was a monoclonal antibody, TS-19, that
specifically binds to the ectodermal epithelial cells
of the tentacles. The second was an antiserum against
the peptide Arg-Phe-amide (RFamide), which in the
head of hydra is specific to the sensory cells of the
hypostomal apex and the ganglion cells of the lower
hypostome and tentacles. The TS-19 expression and
the ganglion cells with RFamide-like immunoreac-
tivity (RLI) arose first at the apex and spread radially.
Once the tentacles began evaginating in a ring, both
the TS-19 antigen and RLI+ ganglion cells gradually
disappeared from the presumptive hypostome area
and RLI+ sensory cells appeared at the apex. By
tracking tissue movements during morphogenesis it
became clear that the apical cap, in which these
changes took place, did not undergo tissue turnover.
The implications of this tentacle-like stage for pattern-
ing the two-part head are discussed.
Key words: hydra, regeneration, pattern formation, two-
part pattern, head, monoclonal antibody.
Introduction
The basic structure of hydra is a hollow cylinder
composed of two tissue monolayers, an ectoderm and
an endoderm separated by a thin extracellular matrix,
the mesoglea. At the base of the cylinder is a holdfast,
which is simply a disc of ectodermal cells secreting
adhesive substances. The head, however, is a more
complicated two-part structure. The upper half is a
smooth dome or cone, the hypostome, that opens to
serve as a mouth. The lower half is the tentacle zone
from which six or seven tentacles protrude.
When the head is removed from an animal a new
head regenerates. Much has already been learned
about the patterning process, such as the factors
affecting its location, as well as information on its
properties and kinetics as it develops (see Bode &
Bode, 1984£> for review). However, most analyses
yielded information only on the presumptive head as
a unit. An important question concerning this process
is how the two parts of the head dome arise. Recent
observations on tentacle regeneration in adult bud-
ding animals and the most common abnormalities
that result have suggested a possible sequence of
events (Bode & Bode, 1987).
The apical end heals over rapidly after decapi-
tation. After one day of regeneration the first one or
two tentacles are visible in some animals. These
occasionally emerge from a small area at the apex.
During the next two days new tentacles appear in
more basal positions, forming a ring around the
dome. Some of the early tentacles may remain above
the ring, well within the hypostome area where the
mouth would normally open. Occasionally regener-
ation is incomplete and only a single tentacle forms at
the apical end.