Caenorhabditis elegans MES-3 Is a Target of GLD-1 and Functions Epigenetically in Germline Development

Caenorhabditis elegans MES-3 Is a Target of GLD-1 and Functions Epigenetically in Germline Development

Lei Xu^a, Janet Paulsen^a, Young Yoo^b, Elizabeth B. Goodwin^c, and Susan Strome^a
^a Department of Biology, Indiana University, Bloomington, Indiana 47405,
^b Department of Cell and Molecular Biology, Northwestern University, Chicago, Illinois 60611
^c Genetics Department, University of Wisconsin, Madison, Wisconsin 53706

Corresponding author: Susan Strome, Department of Biology, Indiana University, Bloomington, IN 47405., sstrome{at}bio.indiana.edu (E-mail)

Communicating editor: T. C. KAUFMAN

The maternal-effect sterile (MES) proteins are maternally suppliedregulators of germline development in Caenorhabditis elegans.In the hermaphrodite progeny from mes mutant mothers, the germlinedies during larval development. On the basis of the similaritiesof MES-2 and MES-6 to known transcriptional regulators and onthe basis of the effects of mes mutations on transgene expressionin the germline, the MES proteins are predicted to be transcriptionalrepressors. One of the MES proteins, MES-3, is a novel proteinwith no recognizable motifs. In this article we show that MES-3is localized in the nuclei of embryos and germ cells, consistentwith its predicted role in transcriptional regulation. Its distributionin the germline and in early embryos does not depend on thewild-type functions of the other MES proteins. However, itsnuclear localization in midstage embryos and its persistencein the primordial germ cells depend on wild-type MES-2 and MES-6.These results are consistent with biochemical data showing thatMES-2, MES-3, and MES-6 associate in a complex in embryos. Thedistribution of MES-3 in the adult germline is regulated bythe translational repressor GLD-1: MES-3 is absent from theregion of the germline where GLD-1 is known to be present, MES-3is overexpressed in the germline of gld-1 mutants, and GLD-1specifically binds the mes-3 3' untranslated region (3' UTR).Analysis of temperature-shifted mes-3(bn21ts) worms and embryosindicates that MES-3 function is required in the mother's germlineand during embryogenesis to ensure subsequent normal germlinedevelopment. We propose that MES-3 acts epigenetically to inducea germline state that is inherited through both meiosis andmitosis and that is essential for survival of the germline.

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