Malakar Bidhan Chandra, Chandramohan Rajanesh, Sethi Vishmita, Gangappa Sreeramaiah N
Department of Biological Sciences, Indian Institute of Science Education and Research Kolkata, Mohanpur, West Bengal, 741246, India.
Centre for Climate and Environmental Studies, Indian Institute of Science Education and Research Kolkata, Mohanpur, West Bengal, 741246, India.
Plant J. 2025 Jul;123(1):e70345. doi: 10.1111/tpj.70345.
Thermomorphogenesis is a plant adaptive response, enabling morphological adjustments to fluctuating ambient temperatures. In Arabidopsis, the bHLH family of transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) plays a central role in promoting thermomorphogenesis, whose activity is negatively regulated by thermosensors EARLY FLOWERING 3 (ELF3) and PHYTOCHROME B (phyB). In response to warm temperatures, PIF4 transcript and protein levels increase to facilitate thermosensory growth. However, the regulatory mechanisms governing PIF4-mediated thermosensory growth remain partially elusive. Here, we demonstrate the role of a B-BOX protein, BBX21, in suppressing thermomorphogenesis through the PIF4 pathway. A mutation in BBX21 (bbx21) results in a longer hypocotyl phenotype accompanied by upregulation in thermoresponsive gene expression, whereas overexpression of BBX21 (BBX21-OE) results in an extremely short hypocotyl phenotype with dampened expression of temperature-responsive genes. Genetic analysis reveals that BBX21 acts upstream of PIF4 to regulate warm temperature-mediated hypocotyl growth. To limit excessive thermomorphogenesis, BBX21 inhibits PIF4 protein accumulation by repressing its transcript accumulation by directly binding to its promoter. Furthermore, our genetic and biochemical data show that the short hypocotyl phenotype of the BBX21-OE line is dependent on ELF3 and phyB. BBX21 enhances the ELF3 and phyB-mediated inhibition of PIF4 activity in SD and LD conditions, respectively, by enhancing their protein activity. Thus, this study elucidates the novel role of BBX21 in suppressing thermomorphogenesis, providing new insights into the molecular mechanism of PIF4-mediated regulation of hypocotyl growth in response to warm temperatures.
热形态建成是一种植物适应性反应，使植物能够根据环境温度波动进行形态调整。在拟南芥中，转录因子光敏色素相互作用因子4（PIF4）所属的bHLH家族在促进热形态建成中起核心作用，其活性受到热感受器早花3（ELF3）和光敏色素B（phyB）的负调控。响应温暖温度时，PIF4的转录本和蛋白质水平会升高，以促进热感生长。然而，PIF4介导的热感生长的调控机制仍部分未知。在此，我们证明了一个B-盒蛋白BBX21通过PIF4途径抑制热形态建成。BBX21的突变（bbx21）导致下胚轴表型变长，同时热响应基因表达上调，而BBX21的过表达（BBX21-OE）则导致下胚轴表型极短，温度响应基因的表达受到抑制。遗传分析表明，BBX21在PIF4上游起作用，调节温暖温度介导的下胚轴生长。为了限制过度的热形态建成，BBX21通过直接结合PIF4的启动子抑制其转录本积累，从而抑制PIF4蛋白积累。此外，我们的遗传和生化数据表明，BBX21-OE系的短下胚轴表型依赖于ELF3和phyB。BBX21分别通过增强ELF3和phyB的蛋白活性，在短日照和长日照条件下增强它们对PIF4活性的抑制作用。因此，本研究阐明了BBX21在抑制热形态建成中的新作用，为PIF4介导的温暖温度响应下胚轴生长调控的分子机制提供了新见解。
