Very‐long‐chain ceramide synthases and PIF4‐mediated auxin signaling act together to modulate thermomorphogenesis in Arabidopsis

Sphingolipids, including ceramides, are structural membrane lipids that function in membrane trafficking and cell polarity. Very-long-chain (VLC) ceramide synthases are essential for plant growth and development, but how VLC ceramide synthases affect developmental programs and their exact roles in plant growth remain unclear. Here, we report that two VLC ceramide synthases, LONGEVITY ASSURANCE GENE ONE HOMOLOG 1 (LOH1) and LOH3, link sphingolipid metabolism and thermomorphogenesis, that is, plant morphogenesis in response to higher temperatures. We found that high ambient temperature (28°C) induced an increase in plant VLC ceramide contents, and defects in LOH1 or LOH3 function inhibited hypocotyl elongation at this temperature. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) potentiates the thermal sensitivity of hypocotyl morphogenesis in a LOH1- and LOH3-dependent manner, directly binding to the LOH1 and LOH3 promoters to enhance their expression. Strikingly, LOH1 and LOH3 also enhance PIF4-dependent transcriptional activation of downstream genes, including PIF4 itself, LOH1, and LOH3. Our study reveals a regulatory mechanism in which PIF4 activates the transcription of LOH1 and LOH3; in turn, LOH1 and LOH3 enhance PIF4 signaling by supporting PIF4-mediated transcriptional responses, thereby controlling plant growth in response to temperature.