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First published online 4 August 2004
doi: 10.1242/dev.01288


Development 131, 4333-4343 (2004)
Published by The Company of Biologists 2004


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TRA-1/GLI controls development of somatic gonadal precursors in C. elegans

Laura D. Mathies1,2, Mara Schvarzstein3, Kristin M. Morphy2, Robert Blelloch4, Andrew M. Spence3 and Judith Kimble1,*

1 Department of Biochemistry and Howard Hughes Medical Institute, University of Wisconsin-Madison, Madison, WI 53706-1544, USA
2 Department of Genetics, North Carolina State University, Raleigh, NC 27695-7614, USA
3 Department of Molecular and Medical Genetics, University of Toronto, Toronto M5S 1A8, Canada
4 Whitehead Institute, Cambridge, MA 02142-1479, USA

* Author for correspondence (e-mail: jekimble{at}facstaff.wisc.edu)

Accepted 5 June 2004

TRA-1/GLI is best known as a master regulator of sex determination in the nematode C. elegans, but its fly and vertebrate homologs (e.g. Ci, GLI) regulate embryonic patterning and cell proliferation. In this paper, we show that TRA-1/GLI controls development of the two somatic gonadal precursors (SGPs) in both XX and XO animals, in addition to its role in sex determination. Normally, SGPs reside at the poles of the gonadal primordium and divide according to intrinsic gonadal axes. In tra-1-null mutants, however, SGPs assume non-polar positions and the polarity of one SGP is reversed. Consistent with its SGP function, TRA-1 protein is present in SGPs during embryogenesis and early larval development. Previous studies have shown that the ehn-3 gene also affects SGP positions, and we report here that tra-1 and ehn-3 interact genetically. Whereas SGPs in tra-1 and ehn-3 single mutants are largely normal and generate many descendants, those in tra-1; ehn-3 double mutants do not mature or divide. Furthermore, tra-1 is a dominant enhancer of the ehn-3 gonadal defect, which includes the enhancement of a weak sexual transformation in the gonad. We cloned ehn-3, and found that it encodes a C2H2 zinc-finger protein. A rescuing EHN-3::GFP reporter is predominantly nuclear and expressed specifically in SGPs. The EHN-3 protein is therefore likely to regulate gene expression. We propose that TRA-1/GLI and EHN-3 have overlapping roles in regulation of multiple steps of SGP development. We speculate that regulation of SGP development may be an evolutionarily ancient role of TRA-1/GLI in nematode development.

Key words: TRA-1, GLI, EHN-3, Cell polarity, Cell proliferation, Gonadogenesis, C. elegans




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