Vertebrate Development Maternal to Zygotic Control (Advances in Experimental Medicine and Biology)

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Spemann in amphibians, and was defined as the “organizer” of axis formation
(Spemann 1918 ; Spemann and Mangold 1924 ). Spemann performed transplantation
experiments in salamanders, demonstrating that the dorsal lip could induce and
organize a normally patterned second body axis when grafted to the opposite (ven-
tral) side of a host gastrula. In this “secondary embryo,” the organizer cells contrib-
uted mostly to notochord themselves, whereas host cells populated the bulk of the
induced axis, which included neural tube, somites, intermediate mesoderm and gut
endoderm. Additional experiments showed that organizer might also contribute to
anteroposterior patterning of the embryo, demonstrating a central role for the orga-
nizer tissue in controlling cell interactions during development.
Although these main findings were firmly established by the 1930s, it was not
until the 1990s that the cellular and molecular mechanisms underlying the action of
the organizer were revisited, resulting in the identification of conserved growth fac-
tor antagonists and transcription factors. The background and history of this work
has been written about exhaustively by Spemann and his contemporaries and later
by modern authors (Spemann 1938 ; Waddington 1940 ; Hamburger 1988 ; Grunz
2004 ). As outlined later in this chapter, the conservation of the organizer extends to
the cellular and genetic levels and largely defines the core mechanisms of early
vertebrate body plan formation.
In contrast to the conservation of the organizer and its components, the ultimate
origins of axial bilateral symmetry in vertebrates are seemingly more diverse. Axis
formation was first extensively studied using amphibians and was linked to cytoplas-
mic localizations in the egg. This was evident in the formation of a natural marker of
the future dorsal side, what came to be called the “gray crescent” (Roux 1888 ). Early
mechanistic studies suggested the crescent formed by rotation of the outer cortex
over the yolky inner cytoplasm (reviewed in Clavert 1962 ; Ancel and Vintemberger
1948 ). This “cortical rotation” was verified by later authors and found to involve the

e

e e

n.p.

dorsal lip

v.l.m. d.m.

bl

c.g.

c.n.s. notochord

gut

c.n.s.

somite notochord

v.l.m.

ab

d

v

ap

v d

Fig. 6.1 Vertebrate axial organization. (a) Diagram of a sagittal section through a Xenopus gas-
trula, showing the involution of the dorsal mesoderm (d.m., dark red) at the dorsal lip. The neural
plate (n.p., blue) overlies the dorsal mesoderm. bl blastocoel, v.l.m. ventrolateral mesoderm
(orange), e endoderm (yellow). (b) Sagittal (left panel) and coronal (right panel) diagrams of a
tailbud-stage Xenopus embryo showing the elongated anterior-to-posterior axis and organization
of tissues within. The neural tube is located dorsally and will form the entire central nervous sys-
tem (c.n.s.). The dorsal mesoderm gives rise to the notochord and somites, ventrolateral mesoderm
(v.l.m.) will form the kidneys, body wall muscles and vascular system. The endoderm forms the
gut and its derivative organs. The cement gland (c.g.), a larval amphibian anchoring structure, is
shown at the anterior end. After Hausen and Riebesell ( 1991 )

6 Vertebrate Axial Patterning: From Egg to Asymmetry