The segmented ectoderm and mesoderm of the leech arise via a stereotyped cell lineage from embryonic stem cells called teloblasts. Each teloblast gives rise to a column of primary blast cell daughters, and the blast cells generate descendant clones that serve as the segmental repeats of their particular teloblast lineage. We have examined the mechanism by which the leech primary blast cell clones acquire segment polarity - i.e. a fixed sequence of positional values ordered along the anteroposterior axis of the segmental repeat. In the O and P teloblast lineages, the earliest divisions of the primary blast cell segregate anterior and posterior cell fates along the anteroposterior axis. Using a laser microbeam, we ablated single cells from both o and p blast cell clones at stages when the clone was two to four cells in length. The developmental fate of the remaining cells was characterized with rhodamine-dextran lineage tracer. Twelve different progeny cells were ablated, and in every case the ablation eliminated the normal descendants of the ablated cell while having little or no detectable effect on the developmental fate of the remaining cells. This included experiments in which we specifically ablated those blast cell progeny that are known to express the engrailed gene, or their lineal precursors. These findings confirm and extend a previous study by showing that the establishment of segment polarity in the leech ectoderm is largely independent of cell interactions conveyed along the anteroposterior axis. Both intercellular signaling and engrailed expression play an important role in the segment polarity specification of the Drosophila embryo, and our findings suggest that there may be little or no conservation of this developmental mechanism between those two organisms.

Reference

Aguinaldo
A. M. A.
,
Turbeville
J. M.
,
Linford
L. S.
,
Rivera
M. C.
,
Garey
J. R.
,
Raff
R. A.
,
Lake
J. A.
(
1997
)
Evidence for a clade of nematodes, arthropods, and other moulting animals.
Nature
387
,
489
493
Blair
S. S.
,
Weisblat
D. A.
(
1984
)
Cell interactions in the developing epidermis of the leech Helobdella triserialis.
Dev. Biol
101
,
318
325
Damen
W. G. M.
,
Hausdorf
M.
,
Seyfarth
E.-A.
,
Tautz
D.
(
1998
)
A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider.
Proc. Nat. Acad. Sci. USA
95
,
10665
10670
De Robertis
E. M.
(
1997
)
The ancestry of segmentation.
Nature
387
,
25
26
de Rosa
R.
,
Grenier
J. K.
,
Andreeva
T.
,
Cook
C. E.
,
Adoutte
A.
,
Akam
M.
,
Carroll
S. B.
,
Balavoine
G.
(
1999
)
Hox genes in branchiopods and priapulids and protostome evolution.
Nature
399
,
772
776
Dawes
R.
,
Dawson
I.
,
Falciani
F.
,
Tear
G.
,
Akam
M.
(
1994
)
Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression.
Development
120
,
1561
1572
DiNardo
S.
,
Sher
E.
,
Heemskerk-Jongens
J.
,
Kassis
J. A.
,
O'Farrell
P. H.
(
1988
)
Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis.
Nature
332
,
604
609
Goldstein
B.
(
1992
)
Induction of gut in Caenorhabditis elegans embryos.
Nature
357
,
255
257
Heemskerk
J.
,
DiNardo
S.
(
1994
)
Drosophila hedgehog acts as a morphogen in cellular patterning.
Cell
76
,
449
460
Ho
R. K.
,
Weisblat
D. A.
(
1987
)
A provisional epithelium in leech embryo: cellular origins and influence on a developmental equivalence group.
Dev. Biol
120
,
520
534
Huang
F. Z.
,
Weisblat
D. A.
(
1996
)
Cell fate determination in an annelid equivalence group.
Development
122
,
1839
1847
Kimmel
C. B.
(
1996
)
Was Urbilateria segmented?.
Trends Genet
12
,
391
392
Kramer
A. P.
,
Weisblat
D. A.
(
1985
)
Developmental neural kinship groups in the leech.
J. Neurosci
5
,
388
407
Lans
D.
,
Wedeen
C. J.
,
Weisblat
D. A.
(
1993
)
Cell lineage analysis of the expression of an engrailed homolog in leech embryos.
Development
117
,
857
871
Lawrence
P. A.
,
Sanson
B.
,
Vincent
J. P.
(
1996
)
Compartments, wingless and engrailed: patterning the ventral epidermis of Drosophila embryos.
Development
122
,
4095
4103
Martindale
M. Q.
,
Shankland
M.
(
1988
)
Developmental origin of segmental differences in the leech ectoderm: survival and differentiation of the distal tubule cell is determined by the host segment.
Dev. Biol
125
,
290
300
Martindale
M. Q.
,
Shankland
M.
(
1990
)
Segmental founder cells of the leech embryo have intrinsic segmental identity.
Nature
347
,
672
674
McGinnis
W.
,
Krumlauf
R.
(
1992
)
Homeobox genes and axial patterning.
Cell
68
,
283
302
Nagy
L. M.
,
Carroll
S.
(
1994
)
Conservation of wingless patterningfunctions in the short-germ embryos of Tribolium castaneum.
Nature
367
,
460
463
Nardelli-Haefliger
D.
,
Bruce
A. E. E.
,
Shankland
M.
(
1994
)
An axial domain of HOM/Hox gene expression is formed by the morphogenetic alignment of independently specified cell lineages in the leech Helobdella.
Development
120
,
1839
1849
Nusslein-Volhard
C.
,
Wieschaus
E.
(
1980
)
Mutations affecting segment number and polarity in Drosophila.
Nature
287
,
795
801
Patel
N. H.
,
Ball
E. E.
,
Goodman
C. S.
(
1992
)
Changing role of even-skipped during the evolution of insect pattern formation.
Nature
357
,
339
342
Patel
N. H.
,
Martin-Blanco
E.
,
Coleman
K. G.
,
Poole
S. J.
,
Ellis
M. C.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of engrailed proteins in arthropods, annelids and chordates.
Cell
58
,
955
968
Patel
N. H.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of engrailed during segmentation in grasshopper and crayfish.
Development
107
,
201
212
Ramirez
F.-A.
,
Wedeen
C. J.
,
Stuart
D. K.
,
Lans
D.
,
Weisblat
D. A.
(
1995
)
Identification of a neurogenic sublineage required for CNS segmentation in an Annelid.
Development
121
,
2091
2097
Seaver
E. C.
,
Shankland
M.
(
2000
)
Leech segmental repeats develop normally in the absence of signals from either anterior or posterior segments.
Dev. Biol
224
,
339
353
Shain
D. H.
,
Stuart
D. K.
,
Huang
F. Z.
,
Weisblat
D. A.
(
2000
)
Segmentation of the central nervous system in leech.
Development
127
,
735
744
Shankland
M.
(
1984
)
Positional determination of supernumerary blast cell death in the leech embryo.
Nature
307
,
541
543
Shankland
M.
(
1987
)
Differentiation of the O and P cell lines in the embryo of the leech. I. Sequential commitment of blast cell sublineages.
Dev. Biol
123
,
85
96
Shankland
M.
(
1987
)
Differentiation of the O and P cell lines in the embryo of the leech. II. Genealogical relationship of descendant pattern elements in alternative developmental pathways.
Dev. Biol
123
,
97
107
Shankland
M.
(
1994
)
Leech segmentation: a molecular perspective.
BioEssays
16
,
801
808
Shankland
M.
,
Bissen
S. T.
,
Weisblat
D. A.
(
1992
)
Description of the Californian leech Helobdella robusta sp. nov., and comparison with H. triserialis on the basis of morphology, embryology, and experimental breeding.
Can. J. Zool
70
,
1258
1263
Shankland
M.
,
Weisblat
D. A.
(
1984
)
Stepwise commitment of blast cell fates during the positional specification of the O and P cell lines in the leech embryo.
Dev. Biol
106
,
326
342
Sommer
R.
(
2000
)
Evolution of nematode development.
Curr. Opin. Gen. Dev
10
,
443
448
Stent
G. S.
,
Kristan
W. B.
Jr
,
Torrence
S. A.
,
French
K. A.
,
Weisblat
D. A.
(
1992
)
Development of the leech nervous system.
Int. Rev. Neurobiol
33
,
109
193
Stuart
D. K.
,
Blair
S. S.
,
Weisblat
D. A.
(
1987
)
Cell lineage, cell death, and the developmental origin of identified serotonin-and dopamine-containing neurons in the leech.
J. Neurosci
7
,
1107
1122
Wedeen
C. J.
,
Weisblat
D. A.
(
1991
)
Segmental expression of an engrailed -class gene during early development and neurogenesis in an annelid.
Development
113
,
805
814
Weisblat
D. A.
,
Blair
S. S.
(
1984
)
Developmental indeterminancy in embryos of the leech Helebodella triserialis.
Dev. Biol
101
,
326
335
Weisblat
D. A.
,
Shankland
M.
(
1985
)
Cell lineage and segmentation in the leech.
Philos. Trans. R. Soc. London Ser. B
312
,
39
56
Zackson
S. L.
(
1984
)
Cell lineage, cell-cell interaction and segment formation in the ectoderm of a glossiphoniid leech embryo.
Dev. Biol
104
,
43
60
This content is only available via PDF.