Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis

Abstract

Ubiquitination is a unique protein degradation system utilized by eukaryotes to efficiently degrade detrimental cellular proteins and control the entire pool of regulatory components. In plants, adaptation in response to various abiotic stresses can be achieved through ubiquitination and the resulting degradation of components specific to these stress signalings. Arabidopsis has more than 1,400 E3 enzymes, indicating E3 ligase acts as a main determinant of substrate specificity. However, as only a minority of E3 ligases related to abiotic stress signaling have been studied in Arabidopsis, the further elucidation of the biological roles and related substrates of newly identified E3 ligases is essential in order to clarify the functional relationship between abiotic stress and E3 ligases. Here, we review the current knowledge and future prospects of the regulatory mechanism and role of several E3 ligases involved in abiotic stress signal transduction in Arabidopsis. As another potential approach to understand how ubiquitination is involved in such signaling, we also briefly introduce factors that regulate the activity of cullin in multisubunit E3 ligase complexes.

Fig. 1.. Ubiquitination process and E3 ligases. (A) Overview of the polyubiquitination process. Ubiquitination requires the sequential action of three enzymes; ubiquitin-activating enzyme (E1), ubiquitin-conjugating enzyme (E2) and ubiquitin ligase (E3). Ubiquitinated substrates are targeted to the 26S proteasome for subsequent degradation. (B) Single subunit and multi-subunit E3 ligases. Based on the E2-interacting region, single subunit E3 ligases can be largely categorized into two types; HECT-type and RING/U-box E3 ligases. Cullin-based E3 ligases are composed of several components; cullin, RBX1, adaptor, and substrate receptor. The resulting complex acts as an E3 ligase in the ubiquitination of substrates. (C) Several types of cullin-based E3 ligases in plants. Cullin 1 assembles into the SCF complex with ASK as an adaptor and F-box protein as a substrate receptor. As cullin 2 was reported to interact with F-box proteins, cullin 2 may be another subunit of the SCF complex (Risseeuw et al., 2003). In the case of cullin 4 complex, DDB1 and DWD proteins are utilized as adaptors and substrate receptors, respectively. Unlike cullin 1 and cullin 4, cullin 3 only requires BTB-containing proteins as substrate receptors without additional adaptor proteins.

Fig. 2.. Abiotic stress signalings and the related E3 ligases. (A, B) Schematic representation of water-deficit stress signaling in the presence or absence of ABA (A) and the involvement of E3 ligases in ABA-mediated drought signaling via AREB/ABF/ ABI5/DPBF bZIP subfamily (B). ‘Substrate modification’ indicates either negative regulation by polyubiquitination or positive regulation by monou-biquitination. (C, D) Simplified scheme of cold signaling pathway (C) and the negative regulation of ICE1 by HOS1 E3 ligase (D). The protein stability of ICE1 is negatively regulated by ubiquitination, whereas its activity is positively regulated by phosphorylation and sumoylation. The activated ICE1 binds to MYCRS in the promoter region of CBF3 and then positively regulates the expression of CBF3 and its downstream genes. ‘P’ and ‘S’ indicates phosphate and small ubiquitin-related modifier (SUMO), respectively.