Abstract
In eukaryotic cells, three nuclear RNA polymerases (RNA pols) carry out the transcription from DNA to RNA, and they all seem to have evolved from a single enzyme present in the common ancestor with archaea. The multiplicity of eukaryotic RNA pols allows each one to remain specialized in the synthesis of a subset of transcripts, which are different in the function, length, cell abundance, diversity, and promoter organization of the corresponding genes. We hypothesize that this specialization of RNA pols has conditioned the evolution of the regulatory mechanisms used to transcribe each gene subset to cope with environmental changes. We herein present the example of the homeostatic regulation of transcript levels versus changes in cell volume. We propose that the diversity and instability of messenger RNAs, transcribed by RNA polymerase II, have conditioned the appearance of regulatory mechanisms based on different gene promoter strength and mRNA stability. However, for the regulation of ribosomal RNA levels, which are very stable and transcribed mainly by RNA polymerase I from only one promoter, different mechanisms act based on gene copy variation, and a much simpler regulation of the synthesis rate.
Highlights
A key step in the central dogma of molecular biology is the transcription of pieces of DNA information into RNA molecules, which will, in some cases, be translated into proteins but will remain, in other cases, as functional non-coding RNAs
In order to generate complex eukaryotes, most evolutionary innovation is expected to occur in periphery subunits, especially in RNA pol II, which specifies the cellular proteome that confers unique characteristics to different cell types through messenger RNA (mRNA) synthesis
RNA pol II targets a large set of differently regulated genes, which requires the capacity to interact with a bigger set of transcription initiation and elongation factors than the other two RNA pols
Summary
A key step in the central dogma of molecular biology is the transcription of pieces of DNA information into RNA molecules, which will, in some cases, be translated into proteins but will remain, in other cases, as functional non-coding RNAs (ncRNAs). Archaeal RNA pol has gained five additional periphery subunits with no homologs in eubacteria but resembling eukaryotic subunits, which stabilize the interactions of polymerase with template DNA, newly synthesized RNA, and different transcription factors to ensure efficient functioning in the transcription cycle (Werner, 2007; Werner and Grohmann, 2011; Fouqueau et al, 2017).
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