High temperature restricts cell division and leaf size by coordination of PIF4 and TCP4 transcription factors

High ambient temperature suppresses Arabidopsis (Arabidopsis thaliana) rosette leaf area and elongates the stem and petiole. While the mechanism underlying the temperature-induced elongation response has been extensively studied, the genetic basis of temperature regulation of leaf size is largely unknown. Here, we show that warm temperature inhibits cell proliferation in Arabidopsis leaves, resulting in fewer cells compared to the control condition. Cellular phenotyping and genetic and biochemical analyses established the key roles of PHYTOCHROME-INTERACTING FACTOR4 (PIF4) and TEOSINTE BRANCHED1/CYCLOIDEA/PCF4 (TCP4) transcription factors in the suppression of Arabidopsis leaf area under high temperature by a reduction in cell number. We show that temperature-mediated suppression of cell proliferation requires PIF4, which interacts with TCP4 and regulates the expression of the cell cycle inhibitor KIP-RELATED PROTEIN1 (KRP1) to control leaf size under high temperature. Warm temperature induces binding of both PIF4 and TCP4 to the KRP1 promoter. PIF4 binding to KRP1 under high temperature is TCP4 dependent as TCP4 regulates PIF4 transcript levels under high temperature. We propose a model where a warm temperature-mediated accumulation of PIF4 in leaf cells promotes its binding to the KRP1 promoter in a TCP4-dependent way to regulate cell production and leaf size. Our finding of high temperature-mediated transcriptional upregulation of KRP1 integrates a developmental signal with an environmental signal that converges on a basal cell regulatory process.