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

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

Research output: Contribution to journalArticle

2 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

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't

Cite this

Crisp, P., 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; 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, P, 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 ; 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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