Additional Layer of Regulation via Convergent Gene Orientation in Yeasts

Abstract

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 mRNA overlapping 3′-ends and can lead to posttranscriptional regulatory events. Here we show that mRNA duplex formation is restricted to convergent genes separated by short intergenic distance, independently of their 3′-untranslated region (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 posttranscriptional 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 messenger-interacting mRNAs forming duplexes in comparison to mRNAs that do not interact (solo mRNAs). Functionally, messenger-interacting mRNAs show limited translational repression upon stress. 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 posttranscriptional regulation is an additional factor that determines the order of coding genes.