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

Bailey, Mark; Srivastava, Anjil Kumar; Conti, Lucio; Nelis, Stuart; Zhang, Cunjin; Florance, Hannah; Love, Andrew J.; Milner, Joel J.; Napier, Richard; Grant, Murray; Sadanandom, Ari

doi:10.1093/jxb/erv468

Cited by 50 publications

(61 citation statements)

References 52 publications

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“…Here, not only did ulp1c/d display stomatal aperture defects, but we also confirmed that QQS was amongst the most up-regulated genes in this mutant. Moreover, ULP1c/d were recently implicated in the modulation of SA biosynthesis and signalling (Bailey et al 2016), further supporting the hypothesis that modulation of stomatal responses by ULP1c/d may involve SA.…”

Section: Ulp1c/d Are Implicated In the Control Of Developmentsupporting

confidence: 67%

SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana

et al. 2016

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Sumoylation is an essential post-translational regulator of plant development and the response to environmental stimuli. SUMO conjugation occurs via an E1-E2-E3 cascade, and can be removed by SUMO proteases (ULPs). ULPs are numerous and likely to function as sources of specificity within the pathway, yet most ULPs remain functionally unresolved. In this report we used loss-of-function reverse genetics and transcriptomics to functionally characterize Arabidopsis thaliana ULP1c and ULP1d SUMO proteases. GUS reporter assays implicated ULP1c/d in various developmental stages, and subsequent defects in growth and germination were uncovered using loss-of-function mutants. Microarray analysis evidenced not only a deregulation of genes involved in development, but also in genes controlled by various drought-associated transcriptional regulators. We demonstrated that ulp1c ulp1d displayed diminished in vitro root growth under low water potential and higher stomatal aperture, yet leaf transpirational water loss and whole drought tolerance were not significantly altered. Generation of a triple siz1 ulp1c ulp1d mutant suggests that ULP1c/d and the SUMO E3 ligase SIZ1 may display separate functions in development yet operate epistatically in response to water deficit. We provide experimental evidence that Arabidopsis ULP1c and ULP1d proteases act redundantly as positive regulators of growth, and operate mainly as isopeptidases downstream of SIZ1 in the control of water deficit responses.

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Section: Ulp1c/d Are Implicated In the Control Of Developmentsupporting

confidence: 67%

SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana

et al. 2016

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“…siz1 or sum1-1 amiR-SUM2) resulting in elevated SA, which promotes transition to flowering especially under short-days. Interestingly, SUMO1/2 or SUMO1/2(DGG) (conjugation-deficient SUMO mutants) overexpressing transgenic plants, or esd4 and ots1 ots2 mutant plants also accumulated higher level of SA and exhibited a severe earlyflowering phenotype under short-days, but a lesser extent under long-days (Murtas et al 2003;Conti et al 2008;van den Burg et al 2010;Bailey et al 2016). Similar to siz1, higher level of SA in esd4 is largely responsible for the early-flowering phenotype of esd4 under short-days (Villajuana-Bonequi et al 2014).…”

Section: Regulation Of Flowering Time By Sumo Conjugation/ Deconjugationmentioning

confidence: 99%

Arabidopsis SUMO protease ASP1 positively regulates flowering time partially through regulating FLC stability

Kong

Luo

et al. 2017

JIPB

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The initiation of flowering is tightly regulated by the endogenous and environment signals, which is crucial for the reproductive success of flowering plants. It is well known that autonomous and vernalization pathways repress transcription of FLOWERING LOCUS C (FLC), a focal floral repressor, but how its protein stability is regulated remains largely unknown. Here, we found that mutations in a novel Arabidopsis SUMO protease 1 (ASP1) resulted in a strong late-flowering phenotype under long-days, but to a lesser extent under short-days. ASP1 localizes in the nucleus and exhibited a SUMO protease activity in vitro and in vivo. The conserved Cys-577 in ASP1 is critical for its enzymatic activity, as well as its physiological function in the regulation of flowering time. Genetic and gene expression analyses demonstrated that ASP1 promotes transcription of positive regulators of flowering, such as FT, SOC1 and FD, and may function in both CO-dependent photoperiod pathway and FLC-dependent pathways. Although the transcription level of FLC was not affected in the loss-of-function asp1 mutant, the protein stability of FLC was increased in the asp1 mutant. Taken together, this study identified a novel bona fide SUMO protease, ASP1, which positively regulates transition to flowering at least partly by repressing FLC protein stability.

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“…In addition to the phytopathogen-injected effector proteases that mediate deSUMOylation in order to alter plant defence responses, plant endogenous SUMO proteases are also known to play integral roles in the regulation of the defence responses (Bailey et al, 2016). Increased amounts of global SUMO conjugation in the ots1ots2 double mutant coincided with enhanced resistance to Pst DC3000 and elevated levels of SA relative to wild-type plants (Bailey et al, 2016). OTS1 and OTS2 limit SA biosynthesis by suppressing ISOCHORISMATE SYNTHASE1 (ICS1) expression.…”

Section: Sumo In Plant Defence Responsesmentioning

confidence: 99%

“…Similar to ubiquitination, the small ubiquitin-like modifier (SUMO), another potent post-translational protein modification system (Vierstra, 2012), is also capable of modulating target protein stability, interaction with partner proteins and subcellular localization (Wilkinson and Henley, 2010). Since its discovery in plants, SUMO has been associated with many different biological processes, such as growth, flowering, light signalling, abiotic stress responses and responses to pathogen infection (Bailey et al, 2016;Conti et al, 2008;Kurepa et al, 2003;Lee et al, 2007;Murtas et al, 2003;Sadanandom et al, 2015). Notably, one of the main classes of targets of SUMO modification is the transcription factors that coordinate transcriptional regulation during developmental and defence processes (Miller et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth–defence balance

Verma

Croley

Sadanandom

2018

Molecular Plant Pathology

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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.

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

Cited by 50 publications

References 52 publications

SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana

SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana

Arabidopsis SUMO protease ASP1 positively regulates flowering time partially through regulating FLC stability

Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth–defence balance

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