Plant SUMO E3 Ligases: Function, Structural Organization, and Connection With DNA

Abstract

Protein modification by the small ubiquitin-like modifier (SUMO) plays an important role in multiple plant processes, including growth, development, and the response to abiotic stresses. Mechanistically, SUMOylation is a sequential multi-enzymatic process where SUMO E3 ligases accelerate SUMO conjugation while also influencing target identity and interactions. This review explores the biological functions of plant SUMO E3 ligases [SAP AND MIZ1 DOMAIN-CONTAINING LIGASE (SIZs), METHYL METHANESULFONATE-SENSITIVITY PROTEIN 21 (MMS21s), and PROTEIN INHIBITOR OF ACTIVATED STAT-LIKE (PIALs)] in relation to their molecular activities and domains. We also explore the sub-cellular localization of SUMO E3 ligases and review evidence suggesting a connection between certain SUMO E3 ligases and DNA that contributes to gene expression regulation.

Keywords: DNA-binding proteins; SUMO E3 ligases; SUMOylation; abiotic stress; structure-function analysis.

Figure 1

Plant SUMO E3 ligases, organizations, and structures. (A) Structure of a complex between SUMO and a SUMO interacting motif (SIM). In this structure, the β-sheet of SUMO (orange) from Saccharomyces cerevisiae is complemented by a β strand (gray) of RANBP2 (PDB 1Z5S) in an antiparallel orientation. (B) SUMOylation conjugation cascade where E1, E2, and E3, respectively, designate an E1-conjugating enzyme (pale yellow), an E2-conjugation enzyme (purple), and an E3-ligase (green). GG represents the di-glycine motif located at the C-terminal end of SUMO. (C) Schematic representation of the three types of SUMO E3 ligases found in plants. As representative members of each class, we chose Arabidopsis thaliana SIZ1 (top), PIAL2 (middle), and MMS21 (bottom). Domains are illustrated by boxes, whereas motifs are depicted by vertical lines. Domains present in plant SUMO E3 ligases include the SAF-A/B, Acinus, and PIAS (SAP) domain, the plant homeodomain (PHD), the PINIT domain, and the SP-RING domain. Historically, the SIM of SIZ1 has been referred to as the SXS motif (Minty et al., 2000). Although a SXS motif is well conserved in plants, this motif is actually part of a C-terminal extension of the SIM (Park et al., 2011). Studies in other systems have indeed shown that the serine residues can be targeted by phosphorylation and that this phosphorylation increases the strength of SUMO-SIM interaction by promoting interactions with a basic patch on SUMO (Chang et al., 2011; Anamika and Spyracopoulos, 2015; Cappadocia et al., 2015a). (D) Crystal structure of a SUMO~E2/SIZ1 complex from S. cerevisiae in a configuration prompt for catalysis (PDB 5JNE). The different domains of SIZ1 are in cartoon and surface representation and are colored as in (C). E2 and SUMO are in cartoon representation in blue and orange, respectively. A gray sphere represents a zinc ion that stabilizes the SP-RING domain, whereas a yellow sphere represents the position of the catalytic cystine within the E2 active site. (E) Solution structure of the SAP domain of Oryza sativa (PDB 2RNO). The domain is in cartoon representation and is colored as in (C). Domain termini are indicated as « N » and « C ». (F) Solution structure of the PHD domain of O. sativa (PDB 2RSD). The domain is in cartoon representation and is colored as in (C). Domain termini are indicated as « N » and « C ».