Regulation of Maternal Transcript Destabilization During Egg Activation in Drosophila

Corresponding author: Howard D. Lipshitz, Research Institute, The Hospital for Sick Children, 555 University Ave., Toronto, ON M5G 1X8, Canada., lipshitz{at}sickkids.ca (E-mail)

Communicating editor: T. SCHÜPBACH

In animals, the transfer of developmental control from maternal RNAs and proteins to zygotically derived products occurs at the midblastula transition. This is accompanied by the destabilization of a subset of maternal transcripts. In Drosophila, maternal transcript destabilization occurs in the absence of fertilization and requires specific cis-acting instability elements. We show here that egg activation is necessary and sufficient to trigger transcript destabilization. We have identified 13 maternal-effect lethal loci that, when mutated, result in failure of maternal transcript degradation. All mutants identified are defective in one or more additional processes associated with egg activation. These include vitelline membrane reorganization, cortical microtubule depolymerization, translation of maternal mRNA, completion of meiosis, and chromosome condensation (the S-to-M transition) after meiosis. The least pleiotropic class of transcript destabilization mutants consists of three genes: pan gu, plutonium, and giant nuclei. These three genes regulate the S-to-M transition at the end of meiosis and are thought to be required for the maintenance of cyclin-dependent kinase (CDK) activity during this cell cycle transition. Consistent with a possible functional connection between this S-to-M transition and transcript destabilization, we show that in vitro-activated eggs, which exhibit aberrant postmeiotic chromosome condensation, fail to initiate transcript degradation. Several genetic tests exclude the possibility that reduction of CDK/cyclin complex activity per se is responsible for the failure to trigger transcript destabilization in these mutants. We propose that the trigger for transcript destabilization occurs coincidently with the S-to-M transition at the end of meiosis and that pan gu, plutonium, and giant nuclei regulate maternal transcript destabilization independent of their role in cell cycle regulation.

This article has been cited by other articles:

				B. Benoit, C. H. He, F. Zhang, S. M. Votruba, W. Tadros, J. T. Westwood, C. A. Smibert, H. D. Lipshitz, and W. E. Theurkauf An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition Development, March 15, 2009; 136(6): 923 - 932. [Abstract] [Full Text] [PDF]

				C. Baroux, D. Autran, C.S. Gillmor, D. Grimanelli, and U. Grossniklaus The Maternal to Zygotic Transition in Animals and Plants Cold Spring Harb Symp Quant Biol, February 9, 2009; (2009) sqb.2008.73.053v1. [Abstract] [PDF]

				J. L. Semotok, H. Luo, R. L. Cooperstock, A. Karaiskakis, H. K. Vari, C. A. Smibert, and H. D. Lipshitz Drosophila Maternal Hsp83 mRNA Destabilization Is Directed by Multiple SMAUG Recognition Elements in the Open Reading Frame Mol. Cell. Biol., November 15, 2008; 28(22): 6757 - 6772. [Abstract] [Full Text] [PDF]

				J. Cui, K. L. Sackton, V. L. Horner, K. E. Kumar, and M. F. Wolfner Wispy, the Drosophila Homolog of GLD-2, Is Required During Oogenesis and Egg Activation Genetics, April 1, 2008; 178(4): 2017 - 2029. [Abstract] [Full Text] [PDF]

				S. Y. Grooms, K.-M. Noh, R. Regis, G. J. Bassell, M. K. Bryan, R. C. Carroll, and R. S. Zukin Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J. Neurosci., August 9, 2006; 26(32): 8339 - 8351. [Abstract] [Full Text] [PDF]

				J. X. Yu, Z. Guan, and H. A. Nash The mushroom body defect Gene Product Is an Essential Component of the Meiosis II Spindle Apparatus in Drosophila Oocytes Genetics, May 1, 2006; 173(1): 243 - 253. [Abstract] [Full Text] [PDF]

				J. Z. Morris, A. Hong, M. A. Lilly, and R. Lehmann twin, a CCR4 homolog, regulates cyclin poly(A) tail length to permit Drosophila oogenesis Development, March 15, 2005; 132(6): 1165 - 1174. [Abstract] [Full Text] [PDF]

				M. Kloc and L. D. Etkin RNA localization mechanisms in oocytes J. Cell Sci., January 15, 2005; 118(2): 269 - 282. [Abstract] [Full Text] [PDF]

				X.-H. Zhang, J. M. Axton, J. Drinjakovic, L. Lorenz, H. White-Cooper, and A. D. Renault Spatial and temporal control of mitotic cyclins by the Gnu regulator of embryonic mitosis in Drosophila J. Cell Sci., July 15, 2004; 117(16): 3571 - 3578. [Abstract] [Full Text] [PDF]

				L. A. Lee, D. Van Hoewyk, and T. L. Orr-Weaver The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions Genes & Dev., December 1, 2003; 17(23): 2979 - 2991. [Abstract] [Full Text] [PDF]