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Across all species, transcription factors (TFs) are the most frequent targets of SUMOylation. The effect of SUMO conjugation on the functions of transcription factors has been extensively studied in animal systems, with over 200 transcription factors being documented to be modulated by SUMOylation. This has resulted in the establishment of a number of paradigms that seek to explain the mechanisms by which SUMO regulates transcription factor functions. For instance, SUMO has been shown to modulate TF DNA binding activity; regulate both localization as well as the abundance of TFs and also influence the association of TFs with chromatin. With transcription factors being implicated as master regulators of the cellular signalling pathways that maintain phenotypic plasticity in all organisms, in this review, we will discuss how SUMO mediated regulation of transcription factor activity facilitates molecular pathways to mount an appropriate and coherent biological response to environmental cues.

In recent years, post-translational modification (PTM) of proteins has emerged as a key process that integrates plant growth and response to a changing environment. During the processes of domestication and breeding, plants were selected for various yield and adaptational characteristics. The post-translational modifier small ubiquitin-like modifier (SUMO) protein is known to have a role in the regulation of a number of these characteristics. Using bioinformatics, we mined the genomes of cereal and Brassica crops and their non-crop relatives Arabidopsis thaliana and Brachypodium distachyon for ubiquitin-like protease (ULP) SUMO protease sequences. We discovered that the SUMO system in cereal crops is disproportionately elaborate in comparison with that in B. distachyon. We use these data to propose deSUMOylation as a mechanism for specificity in the SUMO system.

Salinity is one of the major environmental stresses affecting rice production worldwide. Improving rice salt tolerance is a critical step for sustainable food production. Posttranslational modifications of proteins greatly expand proteome diversity, increase functionality and allow quick responses to environmental stresses, all at low cost to the cell. SUMO mediated modification of substrate proteins is a highly dynamic process governed by the balance of activities of SUMO E3 ligases and deconjugating SUMO proteases. In recent years, SUMO (Small Ubiquitin like Modifier) conjugation of proteins has emerged as an influential regulator of stress signaling in the model plant Arabidopsis. However SUMOylation remain largely under studied in crop plants. We recently identified the SUMO protease gene family in rice and demonstrated a role for OsOTS1 SUMO proteases in salt stress. Interestingly, rice plants silencing OsOTS1 also show significantly reduced germination rate. Knockdown of OsOTS1 gene expression affects root growth by primarily reducing cell size rather than cell division.

SUMO (Small Ubiquitin-like Modifier) conjugation onto target proteins has emerged as a very influential class of protein modification systems. SUMO1/2 double mutant plants are nonviable, underlining the importance of SUMO conjugation to plant survival. Once covalently bound, SUMO can alter a conjugated protein's stability and/or function. SUMO conjugation is a highly dynamic process that can be rapidly reversed by the action of SUMO proteases. The balance between the conjugated/deconjugated forms is a major determinant in the modulation of SUMO-target function. Despite the important mechanistic role of SUMO proteases in model plants, until now the identity or the function of these regulatory enzymes has not been defined in any crop plant. In this report, we reveal the ubiquitin-like protease class of SUMO protease gene family in rice (Oryza sativa) and demonstrate a critical role for OsOTS1 SUMO protease in salt stress. OsOTS-RNAi rice plants accumulate high levels of SUMO-conjugated proteins during salt stress and are highly salt sensitive; however, in non-salt conditions, they are developmentally indistinguishable from wild-type plants. Transgenic rice plants overexpressing OsOTS1 have increased salt tolerance and a concomitant reduction in the levels of SUMOylated proteins. We demonstrate that OsOTS1 confers salt tolerance in rice by increasing root biomass. High salinity triggers OsOTS1 degradation, indicating that increased SUMO conjugation in rice plants during salt stress is in part achieved by down-regulation of OTS1/2 activity. OsOTS1 is nuclear localized indicating a direct requirement of OsOTS1-dependent deSUMOylation activity in rice nuclei for salt tolerance., (© 2016 American Society of Plant Biologists. All Rights Reserved.)

Plants have evolved to cope with changing environmental conditions. One way plants achieve this is through post-translational modification of target proteins by ubiquitination and SUMOylation. These post-translational modifiers (PMs) can alter stability, protein-protein interactions, and the overall fate of the protein. Both of these systems have remarkable similarities in terms of the process leading to attachment of the PM to its substrate : having to undertake activation, conjugation, and finally ligation to the target. In the ubiquitin system, there are a vast number of ubiquitin ligase enzymes (E3s) that provide specificity for the attachment of ubiquitin. With the SUMO system, only a small number of SUMO E3 ligases have so far been identified in the fully sequenced plant genomes. In Arabidopsis thaliana, there are only two SUMO E3s, compared to over 1400 ubiquitin E3s, a trend also observed in crop species such as Oryza sativa and Zea mays Recent research indicates that removing SUMO from its substrate by the enzymatically active SUMO proteases is a vital part of this system. A class of SUMO proteases called ubiquitin-like proteases (ULPs) are widespread in all eukaryotes; within plants, both monocot and dicot kingdoms have conserved and divergent ULPs and ULP-like proteases. This paper examines the roles ULPs have in stress responses and highlights the 'fine-tuning' of SUMO attachment/removal in balancing growth versus stress., (© The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

The conjugation of SUMO can profoundly change the behavior of substrate proteins, impacting a wide variety of cellular responses. SUMO proteases are emerging as key regulators of plant adaptation to its environment because of their instrumental role in the SUMO deconjugation process. Here, we describe how to express, purify, and determine SUMO deconjugation activity of a plant SUMO protease.

Plants survive adversity by modulating their growth in response to changing environmental signals. The phytohormone Gibberellic acid (GA) plays a central role in regulating these adaptive responses by stimulating the degradation of growth repressing DELLA proteins which accumulate during stress. The current model for GA signaling describes how this hormone binds to its receptor GID1 so promoting association of GID1 with DELLA, which then undergoes ubiquitin-mediated proteasomal degradation. Recent data revealed that conjugation of DELLAs to the Small Ubiquitin-like Modifier (SUMO) protein enables plants to modulate its abundance during environmental stress. This is achieved by SUMOylated DELLAs sequestering GID1 via its SUMO interacting motif (SIM) allowing non-SUMOylated DELLAs to accumulate leading to growth restraint under stress and potential yield loss. We demonstrate that GID1 proteins across the major cereal crops contain a functional SIM able to bind SUMO1. Site directed mutagenesis and yeast 2 hybrid experiments reveal that it is possible to disrupt the SIM-SUMO interaction motif without affecting the GA dependent DELLA-GID1 interaction and thereby uncoupling SUMO-mediated inhibition from DELLA degradation. Arabidopsis plants overexpressing a SIM mutant allele of GID1 perform better at relieving DELLA restraint than wild-type GID1. This evidence suggests that manipulating the SIM motif in the GA receptor may provide a possible route to developing stress tolerant crops plants.

Summary: The sessile nature of plants requires them to cope with an ever‐changing environment. Effective adaptive responses require sophisticated cellular mechanisms at the post‐transcriptional and post‐translational levels. Post‐translational modification by small ubiquitin‐like modifier (SUMO) proteins is emerging as a key player in these adaptive responses. SUMO conjugation can rapidly change the overall fate of target proteins by altering their stability or interaction with partner proteins or DNA. SUMOylation entails an enzyme cascade that leads to the activation, conjugation and ligation of SUMO to lysine residues of target proteins. In addition to their SUMO processing activities, SUMO proteases also possess de‐conjugative activity capable of cleaving SUMO from target proteins, providing reversibility and buffering to the pathway. These proteases play critical roles in the maintenance of the SUMO machinery in equilibrium. We hypothesize that SUMO proteases provide the all‐important substrate specificity within the SUMO system. Furthermore, we provide an overview of the role of SUMO in plant innate immunity. SUMOylation also overlaps with multiple growth‐promoting and defence‐related hormone signalling pathways, and hence is pivotal for the maintenance of the growth–defence balance. This review aims to highlight the intricate molecular mechanisms utilized by SUMO to regulate plant defence and to stabilize the growth–defence equilibrium. [ABSTRACT FROM AUTHOR]

Conjugation of SUMO (Small Ubiquitin-like Modifier) protein to cellular targets is emerging as a very influential protein modification system. Once covalently bound, SUMO conjugation can change the stability or functionality of its cognate target proteins. SUMO protease can rapidly reverse SUMO conjugation making this modification system highly dynamic. A major factor in the variation of SUMO-target function is the balance between the conjugated/de-conjugated forms. The mechanistic role of these regulatory SUMO proteases in mediating stress responses has not been defined in any crops. In this study, we reveal the role of the SUMO protease, Os OTS1 in mediating tolerance to drought in rice. Os OTS1 depleted transgenic plants accumulate more ABA and exhibit more productive agronomic traits during drought while Os OTS1 overexpressing lines are drought sensitive but ABA insensitive. Drought and ABA treatment stimulates the degradation of Os OTS1 protein indicating that SUMO conjugation is an important response to drought stress in rice achieved through down-regulation of OTS1/2 activity. We reveal that Os OTS1 SUMO protease directly targets the ABA and drought responsive transcription factor Osb ZIP23 for de- SUMOylation affecting its stability. Os OTS- RNAi lines show increased abundance of Osb ZIP23 and increased drought responsive gene expression while Os OTS1 overexpressing lines show reduced levels of Osb ZIP23 leading to suppressed drought responsive gene expression. Our data reveal a mechanism in which rice plants govern ABA-dependant drought responsive gene expression by controlling the stability of Osb ZIP23 by SUMO conjugation through manipulating specific SUMO protease levels. [ABSTRACT FROM AUTHOR]

Small ubiquitin-like modifier proteases 1 and 2 (SUMO1/2) have been linked to the regulation of salicylic acid (SA)-mediated defence signalling in Arabidopsis thaliana. In order to define the role of the SUMO proteases OVERLY TOLERANT TO SALT1 and -2 (OTS1/2) in defence and to provide insight into SUMO1/2-mediated regulation of SA signalling, we examined the status of SA-mediated defences in ots1/2 mutants. The ots1 ots2 double mutant displayed enhanced resistance to virulent Pseudomonas syringae and higher levels of SA compared with wild-type (WT) plants. Furthermore, ots1 ots2 mutants exhibited upregulated expression of the SA biosynthesis gene ICS1 in addition to enhanced SA-responsive ICS1 expression beyond that of WT. SA stimulated OTS1/2 degradation and promoted accumulation of SUMO1/2 conjugates. These results indicate that OTS1 and -2 act in a feedback loop in SA signalling and that de novo OTS1/2 synthesis works antagonistically to SA-promoted degradation, adjusting the abundance of OTS1/2 to moderate SA signalling. Accumulation of SUMO1/2 conjugates coincides with SA-promoted OTS degradation and may play a positive role in SA-mediated signalling in addition to its repressive roles reported elsewhere. [ABSTRACT FROM AUTHOR]

Due to their sessile nature, plants are constantly subjected to various environmental stresses such as drought, salinity, and pathogen infections. Post-translational modifications (PTMs), like SUMOylation, play a vital role in the regulation of plant responses to their environment. The process of SUMOylation typically involves an enzymatic cascade containing the activation, (E1), conjugation (E2), and ligation (E3) of SUMO to a target protein. Additionally, it also requires a class of SUMO proteases that generate mature SUMO from its precursor and cleave it off the target protein, a process termed deSUMOylation. It is now clear that SUMOylation in plants is key to a plethora of adaptive responses. How this is achieved with an extremely limited set of machinery components is still unclear. One possibility is that novel SUMO components are yet to be discovered. However, current knowledge indicates that only a small set of enzymes seem to be responsible for the modification of a large number of SUMO substrates. It is yet unknown where the specificity lies within the SUMO system. Although this seems to be a crucial question in the field of SUMOylation studies, not much is known about the factors that provide specificity. In this review, we highlight the role of the localisation of SUMO components as an important factor that can play a vital role in contributing to the specificity within the process. This will introduce a new facet to our understanding of the mechanisms underlying such a dynamic process. [ABSTRACT FROM AUTHOR]

Plants adapt to heterogeneous soil conditions by altering their root architecture. For example, roots branch when in contact with water by using the hydropatterning response. We report that hydropatterning is dependent on auxin response factor ARF7. This transcription factor induces asymmetric expression of its target gene LBD16 in lateral root founder cells. This differential expression pattern is regulated by posttranslational modification of ARF7 with the small ubiquitin-like modifier (SUMO) protein. SUMOylation negatively regulates ARF7 DNA binding activity. ARF7 SUMOylation is required to recruit the Aux/IAA (indole-3-acetic acid) repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that SUMO-dependent regulation of auxin response controls root branching pattern in response to water availability. [ABSTRACT FROM AUTHOR]

Summary: Plants survive adverse conditions by modulating their growth in response to a changing environment. Gibberellins (GAs) play a key role in these adaptive responses by stimulating the degradation of growth-repressing DELLA proteins. GA binding to its receptor GID1 enables association of GID1 with DELLAs. This leads to the ubiquitin-mediated proteasomal degradation of DELLAs and consequently growth promotion. We report that DELLA-dependent growth control can be regulated independently of GA. We demonstrate that when a proportion of DELLAs is conjugated to the Small Ubiquitin-like Modifier (SUMO) protein, the extent of conjugation increases during stress. We identify a SUMO-interacting motif in GID1 and demonstrate that SUMO-conjugated DELLA binds to this motif in a GA-independent manner. The consequent sequestration of GID1 by SUMO-conjugated DELLAs leads to an accumulation of non-SUMOylated DELLAs, resulting in beneficial growth restraint during stress. We conclude that plants have developed a GA-independent mechanism to control growth. [Copyright &y& Elsevier]