Phytochromes function as thermosensors inArabidopsis

Abstract

Plants are responsive to temperature, and can distinguish differences of 1ºC. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). The mechanisms of temperature perception are however largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm temperature response, and consistent with this, we show in this background that the warm temperature transcriptome 2 becomes de-repressed at low temperatures. We have discovered phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature dependent manner.The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers, integrating temperature information over the course of the night. One Sentence Summary:The plant temperature transcriptome is controlled at night by phytochromes, acting as thermoresponsive transcriptional repressors. Main Text:Plant development is responsive to temperature, and the phenology and distribution of crops and wild plants have already altered in response to climate change (1, 2). In Arabidopsis thaliana, warm temperature-mediated elongation growth and flowering is dependent on the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR4 and 5 (PIF4 and 5) (3-6). Growth at 27ºC reduces the activity of the Evening Complex (EC) resulting in greater PIF4 transcription. The EC is a transcriptional repressor made up of the proteins EARLY FLOWERING3 (ELF3), ELF4 and LUX ARRHYTHMO (LUX) (7-9). To test if the EC is also required for hypocotyl elongation responses below 22ºC, we examined the behavior of elf3-1 and lux-4 at 12 and 17ºC. Hypocotyl elongation in elf3-1 and lux-4 is largely suppressed at lower temperatures (Fig. 1A, B), which is consistent with cold temperatures being able to suppress PIF4 overexpression phenotypes (10). Since PHYTOCHROME B (PHYB) was identified as a QTL for thermal responsiveness and PIF4 activity is regulated by phytochromes (8, 11), we investigated whether these red light receptors control hypocotyl elongation in the range 12 to 22ºC. Plants lacking phytochrome activity (12) show constitutively long hypocotyls at 12ºC and 17ºC. Thus phytochromes are essential for responding to temperature (Fig. 1C, D and Fig. S1).We used transcriptome analysis to determine whether disrupted thermomorphogenesis in phyABCDE is specific for temperature signaling or is a consequence of misregulated growth pathways. To capture diurnal variation in thermoresponsiveness, we sampled seedlings over 24 hours at 22 and 27ºC. Clustering analysis reveals 20 groups of transcripts ( Fig. 2A and Fig. S3; described in supplement). Thermomorphogenesis occurs predominantly at night and is driven by PIF4. Consistent with this, we observe PIF4 is present in cluster 20, which is more highly expressed at 27ºC during darkness. Clusters 15 and 16 represent the other major groups of 3 nighttim...

PIF3 is a negative regulator of theCBFpathway and freezing tolerance inArabidopsis

“…In addition, phyB was shown to interact with EBF1/2 to promote the degradation of EIN3 (45). Given the recent finding that phyB is a thermosensor of ambient temperature (13,14), it will be intriguing to explore whether phyB also serves as a cold sensor that mediates the EBF1/2-PIF3-CBF pathway.…”

“…Intriguingly, two recent reports demonstrated that phyB acts as a thermosensor of ambient temperature (13,14), but the precise role of phytochromes in the cold stress response awaits further investigation. CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) and ELONGATED HYPOCOTYL 5 (HY5), two central regulators of photomorphogenesis, have been shown to integrate light and cold signaling to optimize plant survival under freezing temperatures (15).…”

Light Signaling, Root Development, and Plasticity

“…PIFs are regulated by light, temperature, and the circadian clock, and these cues can lead to PIF degradation by concerted action of the PHYs and the E3-ligase LightResponse Bric-a-Brack/Tramtrack/Broad (Leivar and Monte, 2014;Ni et al, 2014;Jung et al, 2016;Legris et al, 2016). The PHY and CRY photoreceptors can physically interact with specific sets of PIF proteins and thereby regulate PIF phosphorylation.…”

Seasonal Regulation of Petal Number

“…Phytochromes sense light by switching between an inactive and active form. Warm temperatures deplete the active phytochrome pool and disrupt the transcriptional output of phytochrome B signaling (Jung et al, 2016;Legris et al, 2016). In this way, temperature information is perceived and transduced through the light-sensing pathway to regulate thermomorphogenesis.…”

“…Thermosensing is an important function of the red-light photoreceptor phytochrome B in Arabidopsis, particularly at night (Jung et al, 2016;Legris et al, 2016). Phytochromes sense light by switching between an inactive and active form.…”