Fig. 6: A multisensor high-temperature signaling framework for triggering daytime thermomorphogenesis.
Three thermosensory mechanisms – phyB thermal-reversion-dependent, chloroplast-sucrose-mediated, and ELF3-dependent—work collaboratively and converge on the central thermal regulator PIF4 to trigger thermomorphogenesis in the light. a At 21 °C, phyB represses PIF4 accumulation by promoting its degradation, and ELF3 inhibits both PIF4 transcription and PIF4 activity; consequently, PIF4 is repressed at the transcript, protein, and activity levels. In contrast, at 27 °C, thermo-induced starch degradation in the chloroplasts and sucrose production promote PIF4 accumulation by inhibiting phyB-mediated PIF4 degradation. In parallel, the ELF3-dependent inhibition of PIF4 transcription and PIF4 activity is released. The combined induction of PIF4 accumulation and activity triggers the transcriptional activation of growth-relevant PIF4 target genes, including those associated with auxin biosynthesis and signaling, thereby triggering thermomorphogenesis responses such as hypocotyl growth. The accelerated thermal reversion of phyB at high temperatures can also enhance PIF4 stabilization in relatively low light intensities. However, under strong light conditions where the intensity of R light reaches 50 μmol m−2 s−1 or above, because the rate of phyB photoactivation (k1) is significantly higher than that of phyB thermal reversion (kr), the effect of phyB thermal-reversion-dependent thermosensing becomes negligible, leaving only the chloroplast-sucrose-mediated and ELF3-dependent thermosensing mechanisms operational, as shown in the model. b In hmr-5, under intense light conditions, both the phyB-dependent and chloroplast-sucrose-mediated thermosensory mechanisms are eliminated, and thermomorphogenesis is regulated by the ELF3-dependent thermosensing mechanism only. In this scenario, although the level of PIF4 transcripts can still be enhanced by high temperatures, PIF4-mediated thermomorphogenesis is blocked because PIF4 accumulation is repressed by phyB at both temperatures. c In hmr-5 supplemented with sucrose, exogenous sucrose promotes PIF4 accumulation by antagonizing phyB-mediated PIF4 degradation, thereby bypassing the defect in the chloroplast-sucrose-mediated thermosensory mechanism. However, although the levels of PIF4 can be enhanced at both temperatures, sucrose alone cannot trigger thermomorphogenesis at 21 °C because PIF4 activity is still repressed by ELF3. Therefore, in this scenario, thermomorphogenesis is regulated solely by the ELF3-dependent thermosensory mechanism. d In elf3-1, under intense light conditions, only the chloroplast-sucrose-mediated thermosensory mechanism remains operational. As a result, exogenous sucrose can fully turn on thermomorphogenesis at 21 °C. The image elements of chloroplasts, thermometers, and double-stranded DNA were created in BioRender. Chen, M. (2025) https://BioRender.com/9wqzqu2.
