Small Ubiquitin-Like Modifier Proteases OVERLY TOLERANT TO SALT1 and -2 Regulate Salt Stress Responses in Arabidopsis

Abstract

Understanding salt stress signaling is key to producing salt-tolerant crops. The small ubiquitin-like modifier (SUMO) is a crucial regulator of signaling proteins in eukaryotes. Attachment of SUMO onto substrates is reversible, and SUMO proteases, which specifically cleave the SUMO-substrate linkages, play a vital regulatory role during SUMOylation. We have identified two SUMO proteases, OVERLY TOLERANT TO SALT1 (OTS1) and OTS2, which are localized in the nucleus and act redundantly to regulate salt stress responses in Arabidopsis thaliana. ots1 ots2 double mutants show extreme sensitivity to salt. However, under low-salt conditions, ots1 ots2 double mutants are phenotypically similar to wild-type plants. We demonstrate that salt stress induces a dose-dependent accumulation of SUMO1/2-conjugated proteins in Arabidopsis. ots1 ots2 double mutants constitutively accumulate high levels of SUMO1/2-conjugated proteins even under nonstress conditions and show a further dramatic increase in SUMO1/2-conjugated proteins in response to salt stress. Transgenic lines overexpressing OTS1 have increased salt tolerance and a concomitant reduction in the levels of SUMOylated proteins. Conversely, the ectopic expression of the mutant ots1(C526S) protein lacking SUMO protease activity fails to produce a salt-tolerant phenotype. We show that salt directly affects OTS1-dependent signaling by inducing OTS1 protein degradation. Our results indicate a requirement for OTS1 deSUMOylation activity in plant salt tolerance responses.

Quantitative Proteomics Reveals Factors Regulating RNA Biology as Dynamic Targets of Stress-induced SUMOylation in Arabidopsis

“…Refs. 7,[16][17][18].Important with regard to stress protection are observations that the abundance of SUMO conjugates rises dramatically and reversibly when yeast, animals, and plants are exposed to numerous environmental stresses (7,19,20). For example, a substantial increase in conjugates assembled with the SUMO1 and SUMO2 isoforms can be detected within minutes after treating Arabidopsis seedlings to a relatively mild heat shock (37°C), and this can be subsequently reversed upon a return to non-stress temperatures (7).…”

Overexpression of SIZ1 enhances tolerance to cold and salt stresses and attenuates response to abscisic acid in Arabidopsis thaliana

“…Because the abundance of SUMO1/2 conjugates was observed to increase in a salt concentration-dependent manner (Conti et al 2008), sumoylation may be involved in the regulation of salt tolerance. The ots1 ots2 double mutant, which is impaired in SUMO protease activity, exhibits salt sensitivity (Conti et al 2008), and the amount of SUMO1/2 conjugates under salt stress are reduced in ots1 ots2 mutants than in wild type. Thus, the overexpression of SIZ1 may enhance SUMO1/2 conjugates under salt stress, most likely leading to the augmentation of the tolerance to salt stress.…”

Arabidopsis PIAL1 and 2 Promote SUMO Chain Formation as E4-Type SUMO Ligases and Are Involved in Stress Responses and Sulfur Metabolism

“…It remains to be seen how these properties relate to soil-grown plants, which may encounter both stresses at the same time. The SUMO conjugation system has previously been linked to salt stress response, via SUMO-specific proteases OVERLY TOLERANT TO SALT1 (OTS1) and 2 (Conti et al, 2008). Overexpression of either of these two proteases renders Arabidopsis plants more resistant to salt stress.…”

“…Either alone, or with the help of E3 ligases, SCE links the SUMO carboxyl terminus to lysine e-amino groups in the substrate. Analysis of mutants suggests that SUMO conjugation is important for responses to a variety of stresses including drought, low temperature, and pathogens (Catala et al, 2007;Conti et al, 2008;Lee et al, 2007;Miura et al, 2007Miura et al, , 2012Zheng et al, 2012;Li et al, 2013;Zhang et al, 2013) and that sumoylation affects developmental processes such as growth, initiation of flowering, meristem maintenance, gametophyte development, and root architecture (Murtas et al, 2003;Ishida et al, 2009Ishida et al, , 2012van den Burg et al, 2010;Miura et al, 2011;Thangasamy et al, 2011;Ling et al, 2012;Elrouby et al, 2013;Conti et al, 2014;Son et al, 2014).…”