The <i>Arabidopsis</i> E3 SUMO Ligase SIZ1 Regulates Plant Growth and Drought Responses

Catalá, Ramón; Ouyang, Jie; Abreu, Isabel A.; Hu, Yuxin; HakSoo, Seo; Zhang, Xiuren; Chua, Nam‐Hai

doi:10.1105/tpc.106.049981

Cited by 324 publications

(326 citation statements)

References 57 publications

(12 reference statements)

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“…SIZ1 has been shown to modulate gene expression in response to HR, BR, and ABA signaling, as well as during the transition to flowering (22,26,(45)(46)(47)(48). For example, SIZ1 regulates systemicacquired resistance through both NONEXPRESSOR OF PR1 (NPR1) gene-dependent and SA accumulation-dependent pathways (45).…”

Section: Discussionmentioning

confidence: 99%

Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana

Zheng

Schumaker

Guo

2012

Proc. Natl. Acad. Sci. U.S.A.

174

176

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The phytohormone abscisic acid (ABA) plays an essential role in plant development and during the response of the plant to abiotic stress. In this study, we report that the R2R3-type transcription factor MYB30 is involved in the regulation of ABA signaling. Arabidopsis mutants lacking MYB30 are hypersensitive to ABA during germination and seedling growth. A K283R substitution in MYB30 blocks its SUMO E3 ligase SIZ1-mediated sumoylation in Arabidopsis protoplasts, indicating that MYB30 is sumoylated by SIZ1 and that K283 is the principal site for small ubiquitin-like modifier conjugation. Expression of MYB30 K283R in myb30 partially rescues the mutant ABA-hypersensitive phenotype, but expression of wild-type MYB30 complements the mutant phenotype. Overexpression of MYB30 in wild-type results in an ABA-insensitive phenotype, whereas overexpression of MYB30 in the siz1 mutant does not alter siz1 hypersensitivity to ABA. The siz1-2 myb30-2 double-mutant exhibits greater ABA sensitivity than either single mutant, but a mutation in the SIZ1-sumoylated ABI5 transcription factor suppresses the ABA hypersensitivity of myb30-2 to wild-type levels. Our results suggest that coordination of ABI5 and MYB30 sumoylation by SIZ1 may balance gene expression, which is required for regulation of ABA signaling during seed germination.A bscisic acid (ABA) plays important roles throughout the life cycle of the plant, including during seed development and dormancy, seed germination, early seedling development, flowering, and in response to abiotic and biotic stress. Genetic studies have revealed that a number of loci are essential for ABA biosynthesis (1-5), catabolism (6, 7), and signal transduction (8, 9) in plants.A number of studies have focused on understanding ABA signaling from perception to response. Recently, three groups of ABA receptors (ABAR/GUN5, GRGC/GTG, and PYR/PYL/ RCAR) have been identified in Arabidopsis and shown to bind ABA with high affinity (10-14). The various functions and cellular locations of these ABA receptors point to the complexity of ABA signaling. For example, PYR/PYL/RCAR-modulated ABA signaling has been studied extensively and found to involve a double-negative regulatory system that includes the receptor, protein phosphatases (PP2C), and protein kinases (SnRK2) (15, 16).A group of basic leucine zipper transcription factors, including ABI5, serve as the downstream targets of SnRK2 and phosphorylation is correlated with ABI5 transcriptional activity and protein stability (17-19). ABI5 undergoes 26S proteasome-mediated degradation and ABA stabilizes the ABI5 protein (17). Two ABI5 interacting proteins, AFP (ABI5-interacting protein) and KEG (KEEP ON GOING, a RING-finger ubiquitin E3 ligase) are required for ABI5 degradation (20,21). Arabidopsis lacking either gene is hypersensitive to ABA and an abi5 mutation suppresses the ABA sensitivity of both the afp-1 and keg mutants (20,21). Recently it has been shown that ABI5 is sumoylated by the small ubiquitin-like modifier (SUMO) E3 ligase SIZ1 at amino acid ...

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Section: Discussionmentioning

confidence: 99%

Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana

Zheng

Schumaker

Guo

2012

Proc. Natl. Acad. Sci. U.S.A.

174

176

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“…©2011 KSMCB 1 mental responses, including heat shock, pathogen defense, drought and cold tolerance, ABA signaling, flowering, and phosphate deficiency (Catala et al, 2007;Jin et al, 2008;Lee et al, 2007;Miura et al, 2005;2009;Saracco et al, 2007;Yoo et al, 2006). Recently, van den Burg et al (2010) reported that AtSUMO3 acted downstream of SA accumulation, while involvement of AtSUMO1 and AtSUMO2 has been reported in suppressing SA accumulation.…”

Section: Molecules and Cellsmentioning

confidence: 99%

Identification and Molecular Properties of SUMO-Binding Proteins in Arabidopsis

Park

Choi

Park

et al. 2011

Molecules and Cells

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Reversible conjugation of the small ubiquitin modifier (SUMO) peptide to proteins (SUMOylation) plays important roles in cellular processes in animals and yeasts. However, little is known about plant SUMO targets. To identify SUMO substrates in Arabidopsis and to probe for biological functions of SUMO proteins, we constructed 6xHis-3xFLAG fused AtSUMO1 (HFAtSUMO1) controlled by the CaMV35S promoter for transformation into Arabidopsis Col-0. After heat treatment, an increased sumoylation pattern was detected in the transgenic plants. SUMO1-modified proteins were selected after two-dimensional gel electrophoresis (2-DE) image analysis and identified using matrix-assisted laser-desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). We identified 27 proteins involved in a variety of processes such as nucleic acid metabolism, signaling, metabolism, and including proteins of unknown functions. Binding and sumoylation patterns were confirmed independently. Surprisingly, MCM3 (At5G46280), a DNA replication licensing factor, only interacted with and became sumoylated by AtSUMO1, but not by SUMO1ΔGG or AtSUMO3. The results suggest specific interactions between sumoylation targets and particular sumoylation enzymes.

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“…Anthocyanin levels were determined in 2-wk-old plants according to Catala and colleagues (41). ROS accumulation was visualized and quantified in 2-wk-old plants with NBT and DCFH 2 -DA, respectively, as described (42).…”

Section: Methodsmentioning

confidence: 99%

Integration of low temperature and light signaling during cold acclimation response in Arabidopsis

Catalá

Medina

Salinas

2011

Proc. Natl. Acad. Sci. U.S.A.

308

269

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Certain plants increase their freezing tolerance in response to low nonfreezing temperatures, an adaptive process named cold acclimation. Light has been shown to be required for full cold acclimation, although how light and cold signals integrate and cross-talk to enhance freezing tolerance still remains poorly understood. Here, we show that HY5 levels are regulated by low temperature transcriptionally, via a CBF-and ABA-independent pathway, and posttranslationally, via protein stabilization through nuclear depletion of COP1. Furthermore, we demonstrate that HY5 positively regulates cold-induced gene expression through the Z-box and other cisacting elements, ensuring the complete development of cold acclimation. These findings uncover unexpected functions for HY5, COP1, and the Z-box in Arabidopsis response to low temperature, provide insights on how cold and light signals integrate to optimize plant survival under freezing temperatures, and reveal the complexity of the molecular mechanisms plants have evolved to respond and adapt to their fluctuating natural environment.

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The Arabidopsis E3 SUMO Ligase SIZ1 Regulates Plant Growth and Drought Responses

Cited by 324 publications

References 57 publications

Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana

Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana

Identification and Molecular Properties of SUMO-Binding Proteins in Arabidopsis

Integration of low temperature and light signaling during cold acclimation response in Arabidopsis

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