Promoter-pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt

Eukaryotic genomes are pervasively transcribed by RNA polymerase II. Yet, the molecular and biological implications of such a phenomenon are still largely puzzling. Here, we describe noncoding RNA transcription upstream of the Arabidopsis thaliana DOG1 gene, which governs salt stress responses and is a key regulator of seed dormancy. We find that expression of the DOG1 gene is induced by salt stress, thereby causing a delay in seed germination. We uncover extensive transcriptional activity on the promoter of the DOG1 gene, which produces a variety of lncRNAs. These lncRNAs, named PUPPIES, are co-directionally transcribed and extend into the DOG1 coding region. We show that PUPPIES RNAs respond to salt stress and boost DOG1 expression, resulting in delayed germination. This positive role of pervasive PUPPIES transcription on DOG1 gene expression is associated with augmented pausing of RNA polymerase II, slower transcription and higher transcriptional burst size. These findings highlight the positive role of upstream co-directional transcription in controlling transcriptional dynamics of downstream genes.

Automated summary

We investigated noncoding RNA transcription upstream of the Arabidopsis DOG1 gene and found a positive role of co-directional transcription in regulating the expression of the downstream gene. The transcription activity on the promoter of DOG1 gene produced various lncRNAs named PUPPIES, which responded to salt stress and enhanced DOG1 expression. This resulted in delayed seed germination. The positive role of pervasive PUPPIES transcription was associated with pausing of RNA polymerase II, slower transcription, and higher transcriptional burst size.