Abstract
Transcriptome studies on eukaryotic cells have revealed an unexpected abundance and diversity of noncoding RNAs synthesized by RNA polymerase II (Pol II), some of which influence the expression of protein-coding genes. Yet, much less is known about biogenesis of Pol II non-coding RNA than mRNAs. In the budding yeast Saccharomyces cerevisiae, initiation of non-coding transcripts by Pol II appears to be similar to that of mRNAs, but a distinct pathway is utilized for termination of most non-coding RNAs: the Sen1-dependent or “NNS” pathway. Here, we examine the effect on the S. cerevisiae transcriptome of conditional mutations in the genes encoding six different essential proteins that influence Sen1-dependent termination: Sen1, Nrd1, Nab3, Ssu72, Rpb11, and Hrp1. We observe surprisingly diverse effects on transcript abundance for the different proteins that cannot be explained simply by differing severity of the mutations. Rather, we infer from our results that termination of Pol II transcription of non-coding RNA genes is subject to complex combinatorial control that likely involves proteins beyond those studied here. Furthermore, we identify new targets and functions of Sen1-dependent termination, including a role in repression of meiotic genes in vegetative cells. In combination with other recent whole-genome studies on termination of non-coding RNAs, our results provide promising directions for further investigation.
Highlights
The process of transcription termination has a profound influence on the population of RNAs present in a cell, and on a cell’s physiology
A potential limitation of this approach is that associated proteins may be depleted from the nucleus, or multiprotein complexes may be destabilized by the absence of one subunit, leading to uncertainty regarding the factor-specificity of the observed effects
The Sen1-dependent polymerase II (Pol II) transcription termination pathway was discovered two decades ago, but it is clear that we still have much more to learn about its targets and functions
Summary
The process of transcription termination has a profound influence on the population of RNAs present in a cell, and on a cell’s physiology. The mechanisms by which termination influences RNA levels are manifold. Termination-coupled RNA degradation culls nascent transcripts created by pervasive initiation. This culling process appears to be the main pathway for rendering many intrinsically bidirectional promoters functionally unidirectional [1]. Termination of a messenger RNA, called transcription attenuation, provides a way to decrease protein output even when initiation of synthesis of that mRNA is constant or increasing [2,3,4,5]. Failure to terminate an antisense transcript can decrease the level of the corresponding sense transcript by transcriptional interference, or increase the level of the sense transcript by disabling termination-coupled gene silencing [6,7]
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