Phosphorylation-mediated rewiring of the plant ubiquitin system: from core machinery to ubiquitin-like modifications
Guo, Shujuan ; Peng, Yushi ; Qi, Hua ; Yu, Linhui ; Wang, Qiuling
DOI 10.1093/jxb/eraf550
Abstract
Phosphorylation and ubiquitination are pivotal mechanisms that enable plants to coordinate development and environmental adaptation. These two post-translational modifications engage in multi-layered crosstalk with each other. While extensive research has elucidated ubiquitin-mediated control of kinase stability and substrate-level phosphorylation-ubiquitination interplay in plants, recent advances now reveal that phosphorylation directly rewires the core machinery of the plant ubiquitin-proteasome system (UPS) and ubiquitin-like (UBL) pathways. This review focuses on emerging evidence demonstrating that phosphorylation serves as a molecular switch, targeting UPS/UBL components, including E1/E2 enzymes, E3 ligases, deubiquitinases (DUBs), ubiquitin, and UBL modifiers, to dynamically reconfigure plant protein homeostasis. We emphasize phosphorylation-mediated control over E3 ligases through four key mechanisms: substrate interaction modulation; subcellular relocalization; enzymatic activity tuning; and stability regulation. Furthermore, we discuss how phosphorylation extends beyond classical ubiquitination to regulate UBL pathways (SUMOylation, RUBylation, UFMylation, and ATG8ylation). The integration of this regulatory layer provides a new framework for comprehending how phosphorylation globally regulates ubiquitin-dependent biological processes. We also highlight knowledge gaps in plant-specific mechanisms and propose phosphorylation site engineering as a strategy for designing climate-resilient crops through optimization of the ubiquitination machinery.
Phosphorylation directly manipulates the core machinery of the plant ubiquitin system-not just substrates-to control protein homeostasis, revealing a fundamental regulatory mechanism.