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Review
. 2012 Oct;69(19):3269-83.
doi: 10.1007/s00018-012-1094-2. Epub 2012 Aug 19.

SUMO, a heavyweight player in plant abiotic stress responses

Pedro Humberto Castro  1 , Rui Manuel Tavares, Eduardo R Bejarano, Herlânder Azevedo
Affiliations
Review

SUMO, a heavyweight player in plant abiotic stress responses

Pedro Humberto Castro et al. Cell Mol Life Sci. 2012 Oct.

Abstract

Protein post-translational modifications diversify the proteome and install new regulatory levels that are crucial for the maintenance of cellular homeostasis. Over the last decade, the ubiquitin-like modifying peptide small ubiquitin-like modifier (SUMO) has been shown to regulate various nuclear processes, including transcriptional control. In plants, the sumoylation pathway has been significantly implicated in the response to environmental stimuli, including heat, cold, drought, and salt stresses, modulation of abscisic acid and other hormones, and nutrient homeostasis. This review focuses on the emerging importance of SUMO in the abiotic stress response, summarizing the molecular implications of sumoylation and emphasizing how high-throughput approaches aimed at identifying the full set of SUMO targets will greatly enhance our understanding of the SUMO-abiotic stress association.

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Figures

Fig. 1
Fig. 1
The sumoylation pathway. a Three-dimensional (3D) structure of human small ubiquitin-like modifier (SUMO) 1 (acc. no. 1A5R) and ubiquitin (acc. no. 1UBQ), obtained from the Protein Data Bank (www.rcsb.org/pdb/home/home.do/) and visualized using Jmol, an open-source Java viewer for chemical structures in 3D (www.jmol.org/). b The sumoylation cycle is a conserved five-step pathway (involving maturation, E1-activation, E2-conjugation, E3-ligation, deconjugation) and mediates the balance between the conjugated/deconjugated forms of a target protein. SUMO isoforms encode a pre-SUMO peptide that undergoes maturation by ubiquitin-like proteases (ULP). These SUMO-specific cysteine endopeptidases cleave the C-terminal end, exposing a di-glycine (GG) motif. In the presence of ATP, heterodimeric E1 SUMO-activating enzymes 1 and 2 (SAE1, SAE2) promote the C-terminal binding of SUMO to AMP (SUMO-AMP). A SUMO glycine (G) residue is also coupled to a cysteine (C) of the SAE2, through a high-energy thioester bond. The peptide is then conjugated to an E2 SUMO-conjugating enzyme (SCE1), through transesterification of a C residue in the E2. E2s are subsequently capable of transferring SUMO to a target protein. This step is mostly mediated by SUMO E3 ligases, even though E3-independent transfer is possible. An isopeptide bond is generated between the SUMO G residue and the ε-amino group of a lysine (K) side chain in the target protein’s sumoylation consensus motif ψKXE (ψ, large hydrophobic residue; K, lysine; X, any amino acid; E, glutamic acid), although alternative sumoylation sites also exist. ULPs display isopeptidase in addition to endopeptidase activity, deconjugating SUMO from the target. This final step recycles SUMO and, most significantly, mediates the balance between the target’s conjugated/deconjugated forms
Fig. 2
Fig. 2
Annotation and characterization of the predicted plant SUMO targets. a The four major strategies adopted for identifying plant SUMO targets have rendered a total of 768 proteins. b Venn diagram analysis of the three existing SUMO-conjugate studies. c Venn diagram analysis of the four subsets of strategies used to identify SUMO targets. d Scatterplot of enriched gene ontology (GO) terms (biological process) for the subset of SUMO-conjugates. GO functional categorization was performed using VirtualPlant 1.2 software (http://virtualplant.bio.nyu.edu/cgi-bin/vpweb/), using the BioMaps function with a 0.01 p-value cutoff [102]. Exclusion of GO term redundancy and subsequent scatterplot analysis were performed using the REVIGO tool (http://revigo.irb.hr/), with a 0.5 C-value [65]. Bubble size indicates the frequency of the GO term, colored circles indicate GO terms related to stress or nutritional stimuli. The scatterplot represents the cluster representatives in a 2D space (x- and y-axis) derived by applying multidimensional scaling to a matrix of the GO terms’ semantic similarities [65]. # Number of genes within the subset, asterisk non-Arabidopsis genes, MALDI–TOF MS matrix-assisted laser desorption/ionization–time of flight mass spectrometry
Fig. 3
Fig. 3
Molecular aspects of the SUMO-abiotic stress association in Arabidopsis thaliana. a SIZ1 is a positive regulator of basal thermotolerance. Heat shock likely induces sumoylation of several heat shock factors (HSFs), heat shock proteins (HSPs), and WRKYs. Sumoylation of HSFA2 blocks its activity and consequently down-regulates acquired thermotolerance. b Cold stress regulates the transcription factor (TF) ICE1 through SIZ1-dependent sumoylation, antagonizing HOS1-dependent ubiquitination (Ub) and the degradation of ICE1. Sumoylation activates ICE1 inhibiting MYB15 expression and activating the CBF3/DREB1a-regulon. c Salt and drought stress responses seem to be antagonistically regulated by SIZ1 and ULP1c/d. SIZ1 sumoylates and exerts a positive effect on key regulators of the drought response, while ULP1c/d may counteract this effect by removing SUMO from the target. d ABI5, a key TF in the abscisic acid (ABA) signaling pathway, is sumoylated by SIZ1, which antagonizes ABI5-ubiquitination but also inactivates ABI5 TF activity. e Nutrient availability can be controlled by SUMO. SIZ1 sumoylates nitrate reductases NIA1 and NIA2, contributing positively to nitrogen (N) assimilation. In response to inorganic phosphate (Pi) starvation, SIZ1 bi-sumoylates PHR1 and possibly LPR2, activating the expression of the PHR1-regulon and blocking LPR2 function in the remodeling of root architecture under conditions of Pi starvation. In response to excess copper (Cu), SIZ1 sumoylates an unknown target that directly or indirectly regulates expression of YSL1/3, important for metal re-allocation. f Sumoylation impacts on development at various levels, including ABI5-mediated seed dormancy and growth arrest, nutrient homeostasis, and allocation of metal ions
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