Zhang Zhenzhen, Zhang Hongliang, Feng Lei, Wang Antong, Lin Zijie, Tan Cunyi, Gonzalez Efren, Grismer Tarabryn, Xu Shou-Ling, Wang Zhi-Yong
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA; Synthetic Biology Center, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou 350002, China; College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China.
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
Plant Commun. 2025 Jul 14;6(7):101389. doi: 10.1016/j.xplc.2025.101389. Epub 2025 May 28.
Sugar-mediated regulation of hormone signaling is crucial for optimizing growth under normal conditions and ensuring survival during environmental stress. Previous studies have shown that sugar starvation induces the degradation of BRASSINAZOLE RESISTANT 1 (BZR1), the master transcription factor of the brassinosteroid (BR) signaling pathway, thereby inhibiting growth. However, the molecular mechanism linking sugar signaling to BZR1 degradation remains unknown. To identify proteins that mediate starvation-induced BZR1 degradation, we performed a quantitative proteomic analysis of the BZR1 interactome under starvation conditions and identified UBIQUITIN PROTEIN LIGASE 3 (UPL3) as a sugar-regulated protein that promotes BZR1 degradation and regulates growth and survival in response to sugar availability. upl3 mutants showed increased BZR1 accumulation and larger seedling size compared to the wild type under sugar-limiting conditions, but not when grown on sugar-containing medium, which indicates that UPL3 mediates BZR1 degradation and growth inhibition under sugar-limited conditions. Although upl3 mutations promoted growth under short-term starvation, they substantially reduced survival under long-term starvation. The enhanced growth phenotype of upl3 was also observed when target of rapamycin (TOR) was inactivated, but not when BR biosynthesis was blocked, suggesting that UPL3 acts downstream of sugar-TOR signaling to regulate BZR1 degradation. Furthermore, UPL3 protein levels increased post-transcriptionally in response to starvation and TOR inhibition, and decreased upon sugar treatment. Our study identifies UPL3 as a key molecular link between sugar signaling and BR signaling. We propose that sugar-TOR signaling inhibits UPL3 to promote BZR1 accumulation and growth, thereby optimizing plant growth and survival in response to sugar availability.
糖介导的激素信号调控对于在正常条件下优化生长以及确保在环境胁迫期间的存活至关重要。先前的研究表明，糖饥饿诱导油菜素类固醇（BR）信号通路的主转录因子BRASSINAZOLE RESISTANT 1（BZR1）降解，从而抑制生长。然而，将糖信号与BZR1降解联系起来的分子机制仍然未知。为了鉴定介导饥饿诱导的BZR1降解的蛋白质，我们在饥饿条件下对BZR1相互作用组进行了定量蛋白质组学分析，并鉴定出泛素蛋白连接酶3（UPL3）作为一种糖调节蛋白，其促进BZR1降解并响应糖可用性调节生长和存活。与野生型相比，在糖限制条件下，upl3突变体在含糖培养基上生长时BZR1积累增加且幼苗尺寸更大，但在含糖培养基上生长时则不然，这表明UPL3在糖限制条件下介导BZR1降解和生长抑制。尽管upl3突变在短期饥饿下促进了生长，但它们在长期饥饿下显著降低了存活率。当雷帕霉素靶蛋白（TOR）失活时也观察到了upl3增强的生长表型，但当BR生物合成被阻断时则未观察到，这表明UPL3在糖 - TOR信号下游起作用以调节BZR1降解。此外，UPL3蛋白水平在转录后响应饥饿和TOR抑制而增加，在糖处理时降低。我们的研究将UPL3鉴定为糖信号和BR信号之间的关键分子联系。我们提出糖 - TOR信号抑制UPL3以促进BZR1积累和生长，从而响应糖可用性优化植物生长和存活。
