High temperature limits leaf size via direct control of cell cycle by coordinated functions of PIF4 and TCP4

Abstract

High ambient temperature suppresses Arabidopsis rosette leaf area, in contrast to elongation of stem and petiole. While the mechanism underlying temperature-induced elongation response is extensively studied, the genetic basis of temperature-regulation of leaf size is largely unknown. Here we show that warm temperature inhibits cell proliferation in the Arabidopsis leaves resulting in fewer cells compared to the control condition. Cellular phenotyping, genetic, and biochemical analyses established the key roles of PIF4 and 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 PHYTOCHROME INTERACTING FACTOR 4 (PIF4). PIF4 interacts with TEOSINTE BRANCHED1/CYCLOIDEA/PCF4 (TCP4) and regulates the expression of cell cycle inhibitor, KIP-RELATED PROTEIN 1 (KRP1), to control the 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 levels under high temperature. We propose a model where a warm temperature-mediated accumulation of PIF4 in the 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. One sentence summaryHigh ambient temperature suppresses Arabidopsis leaf area by reducing cell proliferation via PIF4- and TCP4-dependent transcription control of KRP1.