Cotranscriptional splicing is required in the cold to produce <i>COOLAIR</i> isoforms that repress <i>Arabidopsis FLC</i>.

Abstract

Plants use seasonal cold to time the transition to reproductive development. Short- and long-term cold exposure is registered via parallel transcriptional shutdown and Polycomb-dependent epigenetic silencing of the <i>Arabidopsis thaliana</i> major flowering repressor locus <i>FLOWERING LOCUS C</i> (<i>FLC</i>). The cold-induced antisense transcripts (<i>COOLAIR</i>) determine the dynamics of <i>FLC</i> transcriptional shutdown, but the thermosensory mechanisms are still unresolved. Here, through a forward genetic screen, we identify a mutation that perturbs cold-induced <i>COOLAIR</i> expression and <i>FLC</i> repression. The mutation is a hypomorphic allele of SUPPRESSORS OF MEC-8 AND UNC-52 1 (SMU1), a conserved subunit of the spliceosomal B complex. SMU1 interacts in vivo with the proximal region of nascent <i>COOLAIR</i> and RNA 3' processing/cotranscriptional regulators and enhances <i>COOLAIR</i> proximal intron splicing to promote specific <i>COOLAIR</i> isoforms. SMU1 also interacts with ELF7, an RNA Polymerase II Associated Factor (Paf1) component and limits <i>COOLAIR</i> transcription. Cold thus changes cotranscriptional splicing/RNA Pol II functionality in an SMU1-dependent mechanism to promote two different isoforms of <i>COOLAIR</i> that lead to reduced <i>FLC</i> transcription. Such cotranscriptional mechanisms are emerging as important regulators underlying plasticity in gene expression.