A meiotic gene regulatory cascade driven by alternative fates for newly synthesized transcripts

To determine the relative importance of transcriptional regulation versus RNA processing and turnover during the transition from proliferation to meiotic differentiation in the fission yeast Schizosaccharomyces pombe, we analyzed temporal profiles and effects of RNA surveillance factor mutants on ex...

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Bibliographic Details
Published in:Molecular biology of the cell 2011-01, Vol.22 (1), p.66-77
Main Authors: Cremona, Nicole, Potter, Kristine, Wise, Jo Ann
Format: Article
Language:English
Subjects:
Forkhead Transcription Factors - metabolism
Gene Expression Regulation, Fungal
Genes, Regulator
Meiosis - genetics
Mutation
Polyadenylation
Regulatory Elements, Transcriptional
Reverse Transcriptase Polymerase Chain Reaction
RNA Processing, Post-Transcriptional
RNA Splicing
RNA Stability
RNA, Fungal - genetics
RNA, Fungal - metabolism
Schizosaccharomyces - genetics
Schizosaccharomyces - metabolism
Schizosaccharomyces pombe
Schizosaccharomyces pombe Proteins - genetics
Schizosaccharomyces pombe Proteins - metabolism
Transcription, Genetic
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Summary:To determine the relative importance of transcriptional regulation versus RNA processing and turnover during the transition from proliferation to meiotic differentiation in the fission yeast Schizosaccharomyces pombe, we analyzed temporal profiles and effects of RNA surveillance factor mutants on expression of 32 meiotic genes. A comparison of nascent transcription with steady-state RNA accumulation reveals that the vast majority of these genes show a lag between maximal RNA synthesis and peak RNA accumulation. During meiosis, total RNA levels parallel 3' processing, which occurs in multiple, temporally distinct waves that peak from 3 to 6 h after meiotic induction. Most early genes and one middle gene, mei4, share a regulatory mechanism in which a specialized RNA surveillance factor targets newly synthesized transcripts for destruction. Mei4p, a member of the forkhead transcription factor family, in turn regulates a host of downstream genes. Remarkably, a spike in transcription is observed for less than one-third of the genes surveyed, and even these show evidence of RNA-level regulation. In aggregate, our findings lead us to propose that a regulatory cascade driven by changes in processing and stability of newly synthesized transcripts operates alongside the well-known transcriptional cascade as fission yeast cells enter meiosis.
ISSN:1059-1524
1939-4586
DOI:10.1091/mbc.e10-05-0448