Developmental polarity shapes thermo-induced nastic movements in plants

Directional and non-directional environmental cues are able to induce polar behaviors of plants, which are termed tropic and nastic movements, respectively. While molecular mechanisms underlying the directionality of tropic movements are relatively well studied, it is poorly understood how the polarity of nastic movements is determined in response to non-directional stimuli, such as ambient temperatures. It has recently been shown that thermal induction of leaf hyponasty is stimulated by developmentally programmed polar auxin transport in Arabidopsis. Under warm environments, the PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) transcription factor binds to the promoter of PINOID (PID) gene, whose gene product modulates the polar trafficking of the auxin transporter PIN-FORMED 3 (PIN3). Notably, PIF4 binding to the PID promoter occurs predominantly in the abaxial petiole cells than the adaxial petiole cells, leading to differential PID expression and thus asymmetric auxin accumulation in the petiole cells. In addition, ASYMMETRIC LEAVES 1 (AS1), the well-characterized leaf polarity-determining epigenetic regulator, promotes the PID expression by modulating the patterns of histone 4 acetylation (H4Ac) in the PID chromatin. These observations demonstrate that developmental programming of the thermonastic leaf movement through polar auxin distribution enables plants to bend their leaves upward in response to non-directional thermal stimuli, contributing to cooling plant body temperatures under warm temperature conditions. We propose that a developmentally predetermined polarity plays a major role in governing the directionality of various nastic movements in plants.