Stability of small ubiquitin-like modifier (SUMO) proteases OVERLY TOLERANT TO SALT1 and -2 modulates salicylic acid signalling and SUMO1/2 conjugation in Arabidopsis thaliana.

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.

A functional Small Ubiquitin-like Modifier (SUMO) interacting motif (SIM) in the gibberellin hormone receptor GID1 is conserved in cereal crops and disrupting this motif does not abolish hormone dependency of the DELLA-GID1 interaction.

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.

Small Ubiquitin-like Modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin.

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.

The ubiquitin-proteasome system: central modifier of plant signalling.

Ubiquitin is well established as a major modifier of signalling in eukaryotes. However, the extent to which plants rely on ubiquitin for regulating their lifecycle is only recently becoming apparent. This is underlined by the over-representation of genes encoding ubiquitin-metabolizing enzymes in Arabidopsis when compared with other model eukaryotes. The main characteristic of ubiquitination is the conjugation of ubiquitin onto lysine residues of acceptor proteins. In most cases the targeted protein is rapidly degraded by the 26S proteasome, the major proteolysis machinery in eukaryotic cells. The ubiquitin-proteasome system is responsible for removing most abnormal peptides and short-lived cellular regulators, which, in turn, control many processes. This allows cells to respond rapidly to intracellular signals and changing environmental conditions. This review maps out the roles of the components of the ubiquitin-proteasome system with emphasis on areas where future research is urgently needed. We provide a flavour of the diverse aspects of plant lifecycle where the ubiquitin-proteasome system is implicated. We aim to highlight common themes using key examples that reiterate the importance of the ubiquitin-proteasome system to plants. The future challenge in plant biology is to define the targets for ubiquitination, their interactors and their molecular function within the regulatory context.