The F-box E3 ubiquitin ligase BAF1 mediates the degradation of the brassinosteroid-activated transcription factor BES1 through selective autophagy in Arabidopsis

Abstract

Brassinosteroids (BRs) regulate plant growth, development, and stress responses by activating the core transcription factor BRI1-EMS-SUPPRESSOR1 (BES1), whose degradation occurs through the proteasome and autophagy pathways. The E3 ubiquitin ligase(s) that modify BES1 for autophagy-mediated degradation remain to be fully defined. Here, we identified an F-box family E3 ubiquitin ligase named BES1-ASSOCIATED F-BOX1 (BAF1) in Arabidopsis thaliana. BAF1 interacts with BES1 and mediates its ubiquitination and degradation. Our genetic data demonstrated that BAF1 inhibits BR signaling in a BES1-dependent manner. Moreover, BAF1 targets BES1 for autophagic degradation in a selective manner. BAF1-triggered selective autophagy of BES1 depends on the ubiquitin binding receptor DOMINANT SUPPRESSOR OF KAR2 (DSK2). Sucrose starvation-induced selective autophagy of BES1, but not bulk autophagy, was significantly compromised in baf1 mutant and BAF1-ΔF (BAF1 F-box decoy) overexpression plants, but clearly increased by BAF1 overexpression. The baf1 and BAF1-ΔF overexpression plants had increased BR-regulated growth but were sensitive to long-term sucrose starvation, while BAF1 overexpression plants had decreased BR-regulated growth but were highly tolerant of sucrose starvation. Our results not only established BAF1 as an E3 ubiquitin ligase that targets BES1 for degradation through selective autophagy pathway, but also revealed a mechanism for plants to reduce growth during sucrose starvation.

An ORFeome of rice E3 ubiquitin ligases for global analysis of the ubiquitination interactome

“…Protein degradation experiments were performed via transient protein expression in N. benthamiana leaves [ 49 , 50 ] and rice protoplasts. Agrobacterium cultures carrying plasmids harboring GFP-tagged OsSKIPa , OsNRPD1aC , NRR , rTGA2.1 , OsPAL1 , and their cognate E3 ligase genes fused with HA tag were mixed and co-infiltrated into N. benthamiana leaves.…”

Potential Biotechnological Applications of Autophagy for Agriculture

“…Recently, more transcription factors have been identified in plants which can be potentially used to manipulate the autophagy pathway for stress tolerance. Brassinosteroids (BRs) regulate plant growth, development and stress responses by activating the core transcription factor BRI1-EMS-SUPPRESSOR1 (BES1), whose degradation occurs through the proteasome and autophagy pathways ( Nolan et al, 2017 ; Wang et al, 2021 ). BES1 is targeted for autophagy-mediated degradation by direct interaction with ubiquitin-binding receptor protein DOMINANT SUPPRESSOR OF KAR 2 (DSK2) and is targeted to the autophagy pathway during stress via the interaction of DSK2 with ATG8 ( Nolan et al, 2017 ).…”

“…BES1 is targeted for autophagy-mediated degradation by direct interaction with ubiquitin-binding receptor protein DOMINANT SUPPRESSOR OF KAR 2 (DSK2) and is targeted to the autophagy pathway during stress via the interaction of DSK2 with ATG8 ( Nolan et al, 2017 ). Recently, it has been found that ubiquitin ligase BES1-ASSOCIATED F-BOX 1 (BAF1) interacts with BES1 and mediates its ubiquitination and degradation via selective autophagy ( Wang et al, 2021 ).…”

Integration of multi-omics data reveals interplay between brassinosteroid and TORC signaling in Arabidopsis

“…However, the mechanism and biological implications of this interaction are not clear (Xiong et al, 2017). Under stress conditions such as drought or sucrose starvation, BES1 is ubiquitinated by SINAT2 and/or BAF1 ubiquitin ligases and targeted to selective autophagy through ubiquitin receptor DSK2 to slow down plant growth (Nolan et al, 2017b; Yang et al, 2017; Wang et al, 2021). Moreover, BIN2 has been shown to phosphorylate ubiquitin receptor DSK2 to facilitate its interaction with ATG8 and promote BES1 degradation via selective autophagy (Nolan et al, 2017b).…”