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Symmetry breakage in the development of one-armed gonads in nematodes

Félix, Marie-Anne and Sternberg, Paul W. (1996) Symmetry breakage in the development of one-armed gonads in nematodes. Development, 122 (7). pp. 2129-2142. ISSN 0950-1991.

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Whereas the hermaphrodite gonad of Caenorhabditis elegans has two symmetric arms (didelphy), the female/hermaphrodite gonad of many nematode species features a single anterior arm (monodelphy). We examined how gonadal cell lineages and intercellular signalling evolve to generate these diverse structures. In C. elegans, the two arms develop symmetrically from two somatic precursor cells, Z1 (anterior) and Z4 (posterior). Each first gives rise to one distal tip cell (which promotes arm growth and germ line proliferation), two ovary precursors and three uterine precursors in the center of the developing gonad. In monodelphic species, Z1 and Z4 have different fates. The first visible asymmetry between them is in the relative timing of their divisions, followed by asymmetric cell movements. The putative posterior distal tip cell is then eliminated in all but one species by programmed cell death. In some species the posterior ovary precursors form a small vestigial posterior arm, the post-vulval sac; in other species, they stay undivided, or die. In Cephalobus sp. PS1197, the specific fate of Z4 progeny is induced by Z1 (or its daughters). In the uterus in C. elegans, symmetric lateral signalling between Z1.ppp and renders them equally likely to become the anchor cell, which links the uterus to the vulva. In the different monodelphic species, anchor cell specification is biased, or fully fixed, to a descendant of either Z1 or Z4. Replacement regulation upon anchor cell ablation is conserved in some species, but lost in others, leading to a mosaic-type development. Differentiation between Z1 and Z4 is thus manifested at this later stage in the breakage of symmetry of cell interactions in the ventral uterus.

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Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 1996 The Company of Biologists Limited. Accepted 23 April 1996. We are very grateful to L. Carta and W. Sudhaus for strains, to P. De Ley for species identifications, and to all those who collected soil samples for the Caltech worm collection. We thank members of the laboratory for discussions, and D. Anderson, T. Clandinin, J. Liu, A. Newman, R. Palmer and R. Sommer for comments on the manuscript. This work was supported by fellowships from the European Molecular Biology Organisation and the Human Frontier Science Program. P.W.S. is an investigator with the Howard Hughes Medical Institute.
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European Molecular Biology OrganisationUNSPECIFIED
Human Frontier Science Program (HFSP)UNSPECIFIED
Subject Keywords:gonad; evolution; nematodes; cell lineage; apoptosis; lateral signalling
Issue or Number:7
Record Number:CaltechAUTHORS:20120202-101716190
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:29091
Deposited By: Tony Diaz
Deposited On:24 Feb 2012 17:53
Last Modified:03 Mar 2020 13:01

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