Dealing With Stress: A Review of Plant SUMO Proteases

Abstract

The SUMO system is a rapid dynamic post-translational mechanism employed by eukaryotic cells to respond to stress. Plant cells experience hyperSUMOylation of substrates in response to stresses such as heat, ethanol, and drought. Many SUMOylated proteins are located in the nucleus, SUMOylation altering many nuclear processes. The SUMO proteases play two key functions in the SUMO cycle by generating free SUMO; they have an important role in regulating the SUMO cycle, and by cleaving SUMO off SUMOylated proteins, they provide specificity to which proteins become SUMOylated. This review summarizes the broad literature of plant SUMO proteases describing their catalytic activity, domains and structure, evolution, localization, and response to stress and highlighting potential new areas of research in the future.

Keywords: Cysteine protease; Post-translational modification; SUMO cycle; SUMO protease; Stress; Ubiquitin-like.

Figure 1

A variety of the different effects SUMO can have on a target substrate. A- SUMO can aid interaction with proteins containing a SIM site. B- SUMO can change the cellular localization of a protein—for example, directing the protein to the nucleus. C- SUMO can protect substrates from degradation by blocking lysine residues in substrates that may be ubiquitinated. D- SUMO binding to a protein can alter its structure activating the protein. E- SUMOylated proteins can signal to STuBL proteins to target for degradation via ubiquitination. F- SUMO can block interaction with proteins by blocking binding sites.

Figure 2

The SUMO cycle starts with maturation of immature SUMO by cleaving off the C-terminus using a SUMO peptidase. Mature SUMO is then activated using ATP and a heterodimer of SAE1 and SAE2. The SUMO is then passed to SCE in a conjugation step, and using a SUMO ligase is ligated onto the substrate. This substrate can then be SUMOylated at more than one SUMO site or form a polySUMO chain. Lastly, in the deSUMOylation step, SUMO is removed from the substrate using a SUMO isopeptidase to generate free SUMO.

Figure 3

Arabidopsis UBP6 and UBP7 may be a distant USPL1 homologue. Alignment of human USPL1, zebrafish USPL1, Arabidopsis UBP6, and Arabidopsis UBP7. The red boxes highlighting the conserved residues indicate the catalytic triad.

Figure 4

The location of the active site and length of several different SUMO proteases. The orange box denotes the SIM site in ULP1. The blue oval depicts the location of the C48 active site, the green oval the C97 active site, and the purple oval the C98 active site.

Figure 5

Phylogenetic tree of currently identified SUMO proteases in Arabidopsis. The proteases cluster according to their catalytic triad. Alignments were made using ClustalX and visualized in Jalview. Bootstrap neighbor-Joining trees were made using ClustalX and visualized using MEGA7.

Figure 6

A plant cell featuring the known cellular location of SUMO proteases (black) and their substrates (gray). Organelles with a question mark (red) have no known SUMO proteases or substrates but may have undiscovered SUMO proteases.

Figure 7

An Arabidopsis plant with labeled organs listing the proteases that are known to be present in the organ or effect the organ development.