Dynamic ASK1 proximity networks uncover SCF-dependent and noncanonical roles in ABA and drought adaptation

Abstract

Plants rely on rapid proteome remodeling to withstand fluctuating environmental conditions, yet how the ubiquitin system dynamically coordinates these multilayered responses remains unclear. Here we define the in vivo proximity interactome of ARABIDOPSIS SKP1-LIKE 1 (ASK1), the core adaptor of SCF ubiquitin ligases, under acute abscisic acid (ABA) signaling and prolonged drought. TurboID-based proximity labeling coupled with quantitative proteomics revealed that ASK1 assembles highly condition-specific protein networks, distinguishing canonical SCF modules from broader noncanonical associations with transcriptional, chromatin, translational, vesicle-trafficking, and proteostasis machinery. Acute ABA exposure rapidly recruits F-box proteins and ABA-responsive transcription factors while engaging ribosomal and chromatin modules, whereas drought drives ASK1 into expanded proteostasis and stress-signaling assemblies, including chaperone-cochaperone systems, transcriptional repressors, and autophagy-endomembrane components. Global proteomics shows that ASK1 overexpression enhances accumulation of drought-protective and ABA-responsive proteins while repressing immune and ROS-scavenging pathways, indicating a shift in resource allocation. Together, these results describe ASK1 as a multifunctional proteostasis and signaling hub that integrates SCF-dependent and SCF-independent pathways to coordinate transcriptional, translational, and proteolytic reprogramming during plant adaptation to stress.