Natural temperature fluctuations promote <i>COOLAIR</i> regulation of <i>FLC</i>

Abstract

Plants monitor many aspects of their fluctuating environments to help align their development with seasons. Molecular understanding of how noisy temperature cues are registered has emerged from dissection of vernalization in <i>Arabidopsis</i>, which involves a multiphase cold-dependent silencing of the floral repressor locus <i>FLOWERING LOCUS C</i> (<i>FLC</i>). Cold-induced transcriptional silencing precedes a low probability PRC2 epigenetic switching mechanism. The epigenetic switch requires the absence of warm temperatures as well as long-term cold exposure. However, the natural temperature inputs into the earlier transcriptional silencing phase are less well understood. Here, through investigation of <i>Arabidopsis</i> accessions in natural and climatically distinct field sites, we show that the first seasonal frost strongly induces expression of <i>COOLAIR</i>, the antisense transcripts at <i>FLC</i> Chamber experiments delivering a constant mean temperature with different fluctuations showed the freezing induction of <i>COOLAIR</i> correlates with stronger repression of <i>FLC</i> mRNA. Identification of a mutant that ectopically activates <i>COOLAIR</i> revealed how <i>COOLAIR</i> up-regulation can directly reduce <i>FLC</i> expression. Consistent with this, transgenes designed to knockout <i>COOLAIR</i> perturbed the early phase of <i>FLC</i> silencing. However, all transgenes designed to remove <i>COOLAIR</i> resulted in increased production of novel convergent <i>FLC</i> antisense transcripts. Our study reveals how natural temperature fluctuations promote <i>COOLAIR</i> regulation of <i>FLC</i>, with the first autumn frost acting as a key indicator of autumn/winter arrival.