INTRODUCTION
During mouse gastrulation, cells recruited from the epiblast
ingress through the primitive streak (PS) and are organized into
layers of mesodermal cells that constitute the embryonic and
extraembryonic mesoderm. Although the formation of the
mesoderm has been extensively studied (Hashimoto et al.,
1987, Lawson et al., 1991; Lawson and Pedersen, 1992a,b;
Parameswaran and Tam, 1995; Tam and Beddington, 1987;
Tam et al., 1993, 1997), little is known about the
morphogenetic processes that influence the placement of
mesodermal cells in different parts of the embryonic axis and
the extraembryonic membrane. Fate-mapping studies of the
mesoderm of the gastrulating embryo reveal that cells that are
destined for the extraembryonic mesoderm constitute the major
tissue type in the nascent mesodermal layer. The precursors for
cranial and heart mesoderm are present later in the mesodermal
layer of the mid-streak stage embryo, but are ahead of those
that contribute to the paraxial and lateral mesoderm of the
trunk, which form the bulk of the embryonic mesoderm in the
late-streak embryo (Parameswaran and Tam, 1995; Tam et al.,
1997). These studies also show that the various mesoderm
precursors are distinctly regionalized in the mesodermal germ
layer and their relative position is concordant with the final
location in the fetal body. An examination of the regional
distribution of PS-derived cells in the paraxial mesoderm has
revealed that PS cells are allocated to the somites in a
craniocaudal manner (Tam and Beddington, 1987). Epiblast
cells that are recruited to the PS at successive stages of
gastrulation are also found to be distributed similarly in a
craniocaudal order to the gut endoderm (Tam and Beddington,
1992; Lawson et al., 1987; Lawson and Pedersen, 1986).
During gastrulation, cells in the epiblast and their descendants
are progressively displaced towards the PS where cellular
ingression takes place (Lawson et al., 1991; Lawson and
Pedersen, 1992a). It is possible that cells in the epiblast are
recruited for ingression in a sequential order that is determined
by their geographic proximity to the PS. This may imply that
the position of the cells in the epiblast predisposes the order and
timing of their recruitment and thus their destination in the
anteroposterior axis of the body plan. However, clonal analysis
of epiblast cells has revealed significant overlap in the
distribution in both the ectoderm and the mesoderm along the
anteroposterior body axis of clones arising from cells localized
in different regions of the epiblast (Lawson et al., 1991; Lawson
and Pedersen, 1992b). Indeed, any spatial restriction of clonal
4691 Development 126, 4691-4701 (1999)
Printed in Great Britain © The Company of Biologists Limited 1999
DEV4212
The prospective fate of cells in the primitive streak was
examined at early, mid and late stages of mouse gastrula
development to determine the order of allocation of
primitive streak cells to the mesoderm of the
extraembryonic membranes and to the fetal tissues. At the
early-streak stage, primitive streak cells contribute
predominantly to tissues of the extraembryonic mesoderm
as previously found. However, a surprising observation is
that the erythropoietic precursors of the yolk sac emerge
earlier than the bulk of the vitelline endothelium, which is
formed continuously throughout gastrula development.
This may suggest that the erythropoietic and the
endothelial cell lineages may arise independently of one
another. Furthermore, the extraembryonic mesoderm that
is localized to the anterior and chorionic side of the yolk
sac is recruited ahead of that destined for the posterior and
amnionic side. For the mesodermal derivatives in the
embryo, those destined for the rostral structures such as
heart and forebrain mesoderm ingress through the
primitive streak early during a narrow window of
development. They are then followed by those for the rest
of the cranial mesoderm and lastly the paraxial and lateral
mesoderm of the trunk. Results of this study, which
represent snapshots of the types of precursor cells in the
primitive streak, have provided a better delineation of the
timing of allocation of the various mesodermal lineages to
specific compartments in the extraembryonic membranes
and different locations in the embryonic anteroposterior
axis.
Key words: Primitive streak, Cell fate, Mesoderm, Gastrulation,
Mouse
SUMMARY
The orderly allocation of mesodermal cells to the extraembryonic structures
and the anteroposterior axis during gastrulation of the mouse embryo
Simon J. Kinder
1
, Tania E. Tsang
1
, Gabriel A. Quinlan
1
, Anna-Katerina Hadjantonakis
2
, Andras Nagy
2
and
Patrick P. L. Tam
1,
*
1
Embryology Unit, Children’s Medical Research Institute, Locked Bag 23, Wentworthville, NSW 2145, Australia
2
Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario M5G 1X5, Canada
*Author for correspondence (e-mail: ptam@cmri.usyd.edu.au)
Accepted 11 August; published on WWW 6 October 1999