Abstract
Plants use seasonal temperature cues to time the transition to reproduction. In Arabidopsis thaliana, winter cold epigenetically silences the floral repressor locus FLOWERING LOCUS C (FLC) through POLYCOMB REPRESSIVE COMPLEX 2 (PRC2)1. This vernalization process aligns flowering with spring. A prerequisite for silencing is transcriptional downregulation of FLC, but how this occurs in the fluctuating temperature regimes of autumn is unknown2–4. Transcriptional repression correlates with decreased local levels of histone H3 trimethylation at K36 (H3K36me3) and H3 trimethylation at K4 (H3K4me3)5,6, which are deposited during FRIGIDA (FRI)-dependent activation of FLC7–10. Here we show that cold rapidly promotes the formation of FRI nuclear condensates that do not colocalize with an active FLC locus. This correlates with reduced FRI occupancy at the FLC promoter and FLC repression. Warm temperature spikes reverse this process, buffering FLC shutdown to prevent premature flowering. The accumulation of condensates in the cold is affected by specific co-transcriptional regulators and cold induction of a specific isoform of the antisense RNA COOLAIR5,11. Our work describes the dynamic partitioning of a transcriptional activator conferring plasticity in response to natural temperature fluctuations, thus enabling plants to effectively monitor seasonal progression.
Highlights
We analysed how cold influences FRI protein interactions
FRI interacted with subunits of the Mediator complex[12,13], WDR5a and ATX27,9,14, the PAF1 complex[15], general transcription factors[13], RNA-polymerase-II-associated proteins, and many RNA splicing factors and uridine-rich small nuclear ribonucleoproteins[16,17,18], which suggests that FRI has a role in co-transcriptional regulation (Extended Data Table 1)
Like many other co-transcriptional regulators[19,20] we found that FRI–GFP forms nuclear condensates, which were increased in size and number after cold exposure (Fig. 1a, Extended Data Fig. 2a–d)
Summary
In Arabidopsis thaliana, winter cold epigenetically silences the floral repressor locus FLOWERING LOCUS C (FLC) through POLYCOMB REPRESSIVE COMPLEX 2 (PRC2)[1]. This vernalization process aligns flowering with spring. We show that cold rapidly promotes the formation of FRI nuclear condensates that do not colocalize with an active FLC locus. This correlates with reduced FRI occupancy at the FLC promoter and FLC repression. We investigated whether and how FRI function might change in response to fluctuating temperature
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