Additional layer of regulation via convergent gene orientation in yeasts

Abstract

Convergent gene pairs can produce transcripts with complementary sequences. We had shown that mRNA duplexes form in vivo in Saccharomyces cerevisiae via interactions of their 3'-ends and can lead to post-transcriptional regulatory events. Here we show that mRNA duplex formation is restricted to convergent genes separated by short intergenic distance, independently of their 3'-UTR length. We disclose an enrichment in genes involved in biological processes related to stress among these convergent genes. They are markedly conserved in convergent orientation in budding yeasts, meaning that this mode of post-transcriptional regulation could be shared in these organisms, conferring an additional level for modulating stress response. We thus investigated the mechanistic advantages potentially conferred by 3'-UTR mRNA interactions. Analysis of genome-wide transcriptome data revealed that Pat1 and Lsm1 factors, having 3'-UTR binding preference and participating to the remodeling of messenger ribonucleoprotein particles, bind differently these mRNA duplexes in comparison to canonical mRNAs. Functionally, the translational repression upon stress also appears limited on mRNA duplexes. We thus propose that mRNA duplex formation modulates the regulation of mRNA expression by limiting their access to translational repressors. Our results thus show that post-transcriptional regulation is an additional factor that determine the order of coding genes.