The deubiquitinating enzymes UBP12 and UBP13 positively regulate recovery after carbon starvation by modulating BES1 stability in Arabidopsis thaliana

BRI1-EMS-SUPPRESSOR1 (BES1), a core transcription factor in the brassinosteroid (BR) signaling pathway, primarily regulates plant growth and development by influencing BR-regulated gene expression. Several E3 ubiquitin (Ub) ligases regulate BES1 stability, but little is known about BES1 deubiquitination, which antagonizes E3 ligase-mediated ubiquitination to maintain BES1 homeostasis. Here, we report that two Arabidopsis thaliana deubiquitinating enzymes, Ub-SPECIFIC PROTEASE (UBP) 12 and UBP13, interact with BES1. UBP12 and UBP13 removed Ub from polyubiquitinated BES1 to stabilize both phosphorylated and dephosphorylated forms of BES1. A double mutant, ubp12-2w ubp13-3, lacking UBP12 and UBP13 function showed both BR-deficient and BR-insensitive phenotypes, whereas transgenic plants overexpressing UBP12 or UBP13 exhibited an increased BR response. Expression of UBP12 and UPB13 was induced during recovery after carbon starvation, which led to BES1 accumulation and quick recovery of stressed plants. Our work thus establishes a mechanism by which UBP12 and UBP13 regulate BES1 protein abundance to enhance BR-regulated growth during recovery after carbon starvation. Two enzymes deubiquitinate the transcription factor BRI1-EMS-SUPPRESSOR1 to promote its stability and brassinosteroid-regulated growth and thus positively regulate recovery after carbon starvation. In a Nutshell Background: Plants have evolved multiple mechanisms to coordinate growth and stress responses, including global reprogramming of gene expression, RNA processing or sequestration, and post-transcriptional and post-translational modifications. Under stress conditions, plant growth is, in general, placed on hold. During recovery following stress, growth resumes. In contrast to the wealth of studies focusing on stress tolerance, there are relatively few reports on the mechanisms by which plants recover after stress, which is nevertheless crucial as it determines final yield. BRI1-EMS-SUPPRESSOR1 (BES1), a core transcription factor in the brassinosteroid (BR) signaling pathway, as a central regulator for plants in balancing growth and stress response, degradated by several E3 ubiquitin ligases under carbon starvation. Question: We wanted to know whether and which deubiquitinases antagonize the action of E3 ligases to maintain BES1 homeostasis, and the dynamic regulatory mechanism during carbon starvation and recovery after stress via the regulation of BES1 abundance. Findings: We found that the deubiquitinases UBIQUITIN-SPECIFIC PROTEASE12 (UBP12) and UBP13 interact with BES1 and enhance its stability. BES1 abundance decreased in a double mutant lacking UBP12 and UBP13 function and conversely increased in transgenic lines overexpressing UBP12 or UBP13. During carbon starvation, BES1 protein was ubiquitinated and degraded, and UBP12 and UBP13 abundance concomitantly decreased. During recovery after carbon starvation, UBP12 and UBP13 transcription was upregulated and their encoded proteins accumulated, leading to the deubiquitination of BES1 by UBP12 and UBP13 and subsequent BES1 accumulation to promote growth. Next steps: Our work demonstrated a dynamic regulatory mechanism for BES1 during carbon starvation and recovery after carbon starvation. Additional investigations into the transformation of stress to recovery will help us understand the survival strategies of plants.