The FERONIA receptor kinase is required for high humidity responses in Arabidopsis

High humidity greatly influences plant growth and development and triggers adaptive physiological responses such as leaf hyponasty (elongation of leaf petiole and upward leaf movement). Cyclic Nucleotide-Gated Ion Channels 2 and 4 (CNGC2/4), Calmodulin Binding Transcription Activators 2 and 3 (CAMTA2/3)-dependent transcription, and ethylene signaling acting through EIN2 and EIN3/EIL1 are required for high humidity response in Arabidopsis. However, upstream regulators controlling these steps remain unknown. Here, we show that the receptor-like kinase FERONIA and its co-receptor LORELEI-LIKE GPI-ANCHORED PROTEIN1 (LLG1) are required for a large portion of high humidity-associated Arabidopsis transcriptomic changes, including CNGC2, CAMTA-regulated genes, and cell wall remodeling genes, and for high humidity-induced leaf hyponasty. High humidity triggers petiole-localized Ca2+; waves that precede hyponastic leaf movement. The petiole-localized Ca2+ signals were also significantly altered in the fer-4 mutant. Thus, the FERONIA receptor kinase is a critical early regulator of plant responses to high humidity.