RNA polymerase II read-through promotes expression of neighboring genes in SAL1-PAP-XRN retrograde signaling

Peter A. Crisp, Aaron B. Smith, Diep R. Ganguly, Kevin D. Murray, Steven R. Eichten, Anthony A. Millar, Barry J. Pogson

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

In plants, the molecular function(s) of the nucleus-localized 5′-3′ EXORIBONUCLEASES (XRNs) are unclear; however, their activity is reported to have a significant effect on gene expression and SAL1-mediated retrograde signaling. Using parallel analysis of RNA ends, we documented a dramatic increase in uncapped RNA substrates of the XRNs in both sal1 and xrn2xrn3 mutants. We found that a major consequence of reducing SAL1 or XRN activity was RNA Polymerase II 3′ read-through. This occurred at 72% of expressed genes, demonstrating a major genome-wide role for the XRN-torpedo model of transcription termination in Arabidopsis (Arabidopsis thaliana). Read-through is speculated to have a negative effect on transcript abundance; however, we did not observe this. Rather, we identified a strong association between read-through and increased transcript abundance of tan-demly orientated downstream genes, strongly correlated with the proximity (less than 1,000 bp) and expression of the upstream gene. We observed read-through in the proximity of 903 genes up-regulated in the sal1-8 retrograde signaling mutant; thus, this phenomenon may account directly for up to 23% of genes up-regulated in sal1-8. Using APX2 and AT5G43770 as exemplars, we genetically uncoupled read-through loci from downstream genes to validate the principle of read-through-mediated mRNA regulation, providing one mechanism by which an ostensibly posttranscriptional exoribonuclease that targets uncapped RNAs could modulate gene expression.

Original languageEnglish (US)
Pages (from-to)1614-1630
Number of pages17
JournalPlant physiology
Volume178
Issue number4
DOIs
StatePublished - Dec 1 2018

Fingerprint

RNA Polymerase II
DNA-directed RNA polymerase
Gene Expression
gene expression
Genes
RNA
genes
Arabidopsis
exoribonucleases
Exoribonucleases
Torpedo
mutants
major genes
Arabidopsis thaliana
transcription (genetics)
Genome
Messenger RNA
loci
genome

Cite this

Crisp, P. A., Smith, A. B., Ganguly, D. R., Murray, K. D., Eichten, S. R., Millar, A. A., & Pogson, B. J. (2018). RNA polymerase II read-through promotes expression of neighboring genes in SAL1-PAP-XRN retrograde signaling. Plant physiology, 178(4), 1614-1630. https://doi.org/10.1104/pp.18.00758

RNA polymerase II read-through promotes expression of neighboring genes in SAL1-PAP-XRN retrograde signaling. / Crisp, Peter A.; Smith, Aaron B.; Ganguly, Diep R.; Murray, Kevin D.; Eichten, Steven R.; Millar, Anthony A.; Pogson, Barry J.

In: Plant physiology, Vol. 178, No. 4, 01.12.2018, p. 1614-1630.

Research output: Contribution to journalArticle

Crisp, PA, Smith, AB, Ganguly, DR, Murray, KD, Eichten, SR, Millar, AA & Pogson, BJ 2018, 'RNA polymerase II read-through promotes expression of neighboring genes in SAL1-PAP-XRN retrograde signaling', Plant physiology, vol. 178, no. 4, pp. 1614-1630. https://doi.org/10.1104/pp.18.00758
Crisp, Peter A. ; Smith, Aaron B. ; Ganguly, Diep R. ; Murray, Kevin D. ; Eichten, Steven R. ; Millar, Anthony A. ; Pogson, Barry J. / RNA polymerase II read-through promotes expression of neighboring genes in SAL1-PAP-XRN retrograde signaling. In: Plant physiology. 2018 ; Vol. 178, No. 4. pp. 1614-1630.
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