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Open Access Research

Genome-wide analysis of the maternal-to-zygotic transition in Drosophila primordial germ cells

Najeeb U Siddiqui12, Xiao Li1, Hua Luo1, Angelo Karaiskakis1, Huayun Hou13, Thomas Kislinger4, J Timothy Westwood5, Quaid Morris16* and Howard D Lipshitz1*

Author Affiliations

1 Department of Molecular Genetics, University of Toronto, 1 King's College Circle, Toronto, Ontario, Canada M5S 1A8

2 Program in Developmental and Stem Cell Biology, Hospital for Sick Children Research Institute, Toronto Medical Discovery Tower, 101 College Street, Toronto, Ontario, Canada M5G 1L7

3 School of Life Sciences, Peking University, No.5 Yiheyuan Road, Haidian District, Beijing, China 100871

4 University Health Network and Department of Medical Biophysics, University of Toronto, Toronto Medical Discovery Tower, 101 College Street, Toronto, Ontario, Canada M5G 1L7

5 Department of Cell and Systems Biology and Department of Biology, University of Toronto at Mississauga, 3359 Mississauga Road, Mississauga, Ontario, Canada L5L 1C6

6 Banting and Best Department of Medical Research, Terrence Donnelly Centre for Cellular and Biomolecular Research, 160 College Street, Toronto, Ontario, Canada M5S 3E1

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Genome Biology 2012, 13:R11  doi:10.1186/gb-2012-13-2-r11

Published: 20 February 2012

Abstract

Background

During the maternal-to-zygotic transition (MZT) vast changes in the embryonic transcriptome are produced by a combination of two processes: elimination of maternally provided mRNAs and synthesis of new transcripts from the zygotic genome. Previous genome-wide analyses of the MZT have been restricted to whole embryos. Here we report the first such analysis for primordial germ cells (PGCs), the progenitors of the germ-line stem cells.

Results

We purified PGCs from Drosophila embryos, defined their proteome and transcriptome, and assessed the content, scale and dynamics of their MZT. Transcripts encoding proteins that implement particular types of biological functions group into nine distinct expression profiles, reflecting coordinate control at the transcriptional and posttranscriptional levels. mRNAs encoding germ-plasm components and cell-cell signaling molecules are rapidly degraded while new transcription produces mRNAs encoding the core transcriptional and protein synthetic machineries. The RNA-binding protein Smaug is essential for the PGC MZT, clearing transcripts encoding proteins that regulate stem cell behavior, transcriptional and posttranscriptional processes. Computational analyses suggest that Smaug and AU-rich element binding proteins function independently to control transcript elimination.

Conclusions

The scale of the MZT is similar in the soma and PGCs. However, the timing and content of their MZTs differ, reflecting the distinct developmental imperatives of these cell types. The PGC MZT is delayed relative to that in the soma, likely because relief of PGC-specific transcriptional silencing is required for zygotic genome activation as well as for efficient maternal transcript clearance.