Trehalose‐6‐phosphate signaling regulates thermoresponsive hypocotyl growth in Arabidopsis thaliana

• Published in: EMBO reports Vol. 20; no. 10; pp. e47828 - n/a
• Main Authors: Hwang, Geonhee, Kim, Sara, Cho, Jae‐Yong, Paik, Inyup, Kim, Jeong‐Il, Oh, Eunkyoo
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 04.10.2019; Blackwell Publishing Ltd; John Wiley and Sons Inc
• Subjects: Arabidopsis; Arabidopsis - drug effects; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Deficient mutant; EMBO11; EMBO21; EMBO30; Energy balance; Environmental changes; Environmental conditions; Environmental stress; Gene Expression Regulation, Plant - drug effects; Glucose - pharmacology; High temperature; Hypocotyl - growth & development; Hypocotyl - metabolism; Kinases; Models, Biological; Morphogenesis - drug effects; Phosphate; PIF4; Plant growth; Proteasome Endopeptidase Complex - metabolism; Protein Binding - drug effects; Protein Stability - drug effects; Proteolysis - drug effects; Signal transduction; Signal Transduction - drug effects; Signaling; Sucrose - pharmacology; Sugar; Sugar Phosphates - metabolism; Temperature; Temperature effects; thermomorphogenesis; TPS1; Trehalose; Trehalose - analogs & derivatives; Trehalose - metabolism; trehalose‐6‐phosphate; PIF4; thermomorphogenesis; TPS1; trehalose‐6‐phosphate; Arabidopsis; trehalose-6-phosphate
• ISSN: 1469-221X; 1469-3178; 1469-3178
• DOI: 10.15252/embr.201947828

Growth plasticity is a key mechanism by which plants adapt to the ever‐changing environmental conditions. Since growth is a high‐energy‐demanding and irreversible process, it is expected to be regulated by the integration of endogenous energy status as well as environmental conditions. Here, we show that trehalose‐6‐phosphate (T6P) functions as a sugar signaling molecule that coordinates thermoresponsive hypocotyl growth with endogenous sugar availability. We found that the loss of T6P SYNTHASE 1 (TPS1) in Arabidopsis thaliana impaired high‐temperature‐mediated hypocotyl growth. Consistently, the activity of PIF4, a transcription factor that positively regulates hypocotyl growth, was compromised in the tps1 mutant. We further show that, in the tps1 mutant, a sugar signaling kinase KIN10 directly phosphorylates and destabilizes PIF4. T6P inhibits KIN10 activity in a GRIK‐dependent manner, allowing PIF4 to promote hypocotyl growth at high temperatures. Together, our results demonstrate that T6P determines thermoresponsive growth through the KIN10‐PIF4 signaling module. Such regulation of PIF4 by T6P integrates the temperature‐signaling pathway with the endogenous sugar status, thus optimizing plant growth response to environmental stresses. Synopsis Trehalose‐6‐phosphate is a signaling molecule coordinating endogenous sugar availability and plant growth at high temperatures. High temperature‐mediated hypocotyl growth is impaired in trehalose‐6‐phosphate synthase deficient mutants ( tps1 ). In the tps1 mutant, the SnRK1 kinase KIN10 phosphorylates and destabilizes PIF4, which suppresses high temperature‐mediated hypocotyl growth. Trehalose‐6‐phosphate inactivates KIN10 in a GRIK‐dependent manner, which is a negative regulator of PIF4. Graphical Abstract Trehalose‐6‐phosphate is a signaling molecule coordinating endogenous sugar availability and plant growth at high temperatures.