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Poly(A) site choice and Pol2 CTD Serine-5 status govern lncRNA control of phosphate-responsive tgp1 gene expression in fission yeast.

ABSTRACT: Expression of fission yeast glycerophosphate transporter Tgp1 is repressed in phosphate-rich medium and induced during phosphate starvation. Repression is enforced by transcription of the nc-tgp1 locus upstream of tgp1 to produce a long noncoding (lnc) RNA. Here we identify two essential elements of the nc-tgp1 promoter: a TATA box -30TATATATA-23 and a HomolD box -64CAGTCACA-57, mutations of which inactivate the nc-tgp1 promoter and de-repress the downstream tgp1 promoter under phosphate-replete conditions. The nc-tgp1 lncRNA poly(A) site maps to nucleotide +1636 of the transcription unit, which coincides with the binding site for Pho7 (1632TCGGACATTCAA1643), the transcription factor that drives tgp1 expression. Overlap between the lncRNA template and the tgp1 promoter points to transcriptional interference as the simplest basis for lncRNA repression. We identify a shorter RNA derived from the nc-tgp1 locus, polyadenylated at position +508, well upstream of the tgp1 promoter. Mutating the nc-tgp1-short RNA polyadenylation signal abolishes de-repression of the downstream tgp1 promoter elicited by Pol2 CTD Ser5Ala phospho-site mutation. Ser5 mutation favors utilization of the short RNA poly(A) site, thereby diminishing transcription of the lncRNA that interferes with the tgp1 promoter. Mutating the nc-tgp1-short RNA polyadenylation signal attenuates induction of the tgp1 promoter during phosphate starvation. Polyadenylation site choice governed by CTD Ser5 status adds a new level of lncRNA control of gene expression and reveals a new feature of the fission yeast CTD code.

SUBMITTER: Sanchez AM

PROVIDER: S-EPMC5769750 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Poly(A) site choice and Pol2 CTD Serine-5 status govern lncRNA control of phosphate-responsive tgp1 gene expression in fission yeast.

Sanchez Ana M AM Shuman Stewart S Schwer Beate B

RNA (New York, N.Y.) 20171109 2

Expression of fission yeast glycerophosphate transporter Tgp1 is repressed in phosphate-rich medium and induced during phosphate starvation. Repression is enforced by transcription of the nc-tgp1 locus upstream of tgp1 to produce a long noncoding (lnc) RNA. Here we identify two essential elements of the nc-tgp1 promoter: a TATA box -30TATATATA-23 and a HomolD box -64CAGTCACA-57, mutations of which inactivate the nc-tgp1 prom ...[more]

PMID: 29122971

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Project description:The primary structure and phosphorylation pattern of the tandem YSPTSPS repeats of the RNA polymerase II CTD comprise an informational code that coordinates transcription, chromatin modification, and RNA processing. To gauge the contributions of individual CTD coding M-bM-^@M-^\lettersM-bM-^@M-^] to gene expression, we analyzed the poly(A)+ transcriptomes of fission yeast mutants that lack each of the four inessential CTD phosphoacceptors: Tyr1, Ser2, Thr4, and Ser7. There was a hierarchy of CTD mutational effects with respect to the number of dysregulated protein-coding RNAs, with S2A (n=227) >> Y1F (n=71) > S7A (n=58) >> T4A (n=7). The majority of the protein-coding RNAs affected in Y1F cells were coordinately affected by S2A, suggesting that Tyr1-Ser2 constitutes a two-letter code M-bM-^@M-^\wordM-bM-^@M-^]. Y1F and S2A elicited increased expression of genes encoding proteins involved in iron uptake (Frp1, Fip1, Fio1, Str3, Str1, Sib1), without affecting the expression of the genes that repress the iron regulon, implying that Tyr1-Ser2 transduces a repressive signal. Y1F and S2A cells had increased levels of ferric reductase activity and were hypersensitive to phleomycin, indicative of elevated intracellular iron. The T4A and S7A mutations had opposing effects on the phosphate response pathway. T4A reduced the expression of two genes encoding proteins involved in phosphate acquisition (the Pho1 acid phosphatase and the phosphate transporter SPBC8E4.01c), without affecting the expression of known genes that regulate the phosphate response pathway, while S7A increased pho1+ expression. Meiotic genes were enriched among those up-regulated in S7A cells. These results highlight specific cellular gene expression programs that are responsive to distinct CTD cues. Interrogation of the S. pombe transcriptome using polyA+ strand specific RNA sequencing (Illumina HiSeq 2000) in cultures. A total of 16 samples were analysed: two biological repeates of each WT, Y1F, S2A, T4A, S7A,Y1F-S7A, S2A-S7A and T4A-S7A strains

Dataset Information

Poly(A) site choice and Pol2 CTD Serine-5 status govern lncRNA control of phosphate-responsive tgp1 gene expression in fission yeast.

Publications

Poly(A) site choice and Pol2 CTD Serine-5 status govern lncRNA control of phosphate-responsive <i>tgp1</i> gene expression in fission yeast.

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