The epidermis coordinates thermoresponsive growth through the phyB-PIF4-auxin pathway

In plants, an elevation in ambient temperature induces morphological changes including elongation hypocotyls, considered to be adaptive responses to alleviate the heat-induced damages. The high temperature-induced morphological changes are called thermomorphogenesis, which is predominantly regulated by a bHLH transcription factor PIF4. Although PIF4 is expressed in all aerial tissues including the epidermis, mesophyll, and vascular bundle, its tissue-specific functions in thermomorphogenesis are not known. Here, we found that epidermis-specific expression of PIF4 induced constitutive long hypocotyls, while vasculature-specific expression of PIF4 had no effect on hypocotyl growth. Consistently, RNA-Seq and qRT-PCR analyses revealed that auxin responsive genes and growth-related genes were highly activated by epidermal, but not by vascular, PIF4. The epidermal, but not vascular, inactivation of PIF4 by a PIF4 artificial microRNA or a dominant negative form of PIF4 suppressed thermoresponsive gene expression and hypocotyl growth. Additionally, both the block of epidermal auxin signaling and the epidermal overexpression of a thermosensor phytochrome B (phyB) inhibited thermoresponsive growth, indicating that epidermal PIF4-auxin pathway are essential for the temperature responses. We further show that epidermal PIF4 is increased by high temperatures mainly through the transcriptional activation of PIF4. Taken together, our study demonstrates that the epidermis regulates thermoresponsive growth through the phyB-PIF4-auxin pathway. Overall design: Seedlings were grown under white light for 5 days at 20 °C before harvesting for total RNA extraction.