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Nacerddine K., Lehembre F., Bhaumik M., Artus J., Cohen-Tannoudji M., Babinet C., Pandolfi P.P., and Dejean A. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 9 (2005) 769-779
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Saracco SA, Miller MJ, Kurepa J, Vierstra RD: Genetic analysis of sumoylation in Arabidopsis: Heat-induced conjugation of SUMO1 and 2 is essential. Plant Physiol 2007, PMID: 17644626. Authors identify that sumoylation is essential for viability in Arabidopsis. Loss of Arabidopsis SAE2 (SUMO activating enzyme), SCE1 (SUMO conjugating enzyme), or double mutations in SUMO1 and SUMO2 leads to embryonic lethal in early embryo development. Heat-induced SUMO1 and SUMO2 conjugation is mainly facilitated by SUMO E3 ligase AtSIZ1.
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In this study, the authors identify that AtSIZ1 is a SUMO E3 ligase. The mutation in AtSIZ1 caused hyper-response to phosphate deficiency, including cessation of primary root growth, enhanced lateral root and root hair development, and increased anthocyanin accumulation. The work reveals that the MYB transcription factor PHR1 is one of sumoylation target proteins.
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Miura K., Rus A., Sharkhuu A., Yokoi S., Karthikeyan A.S., Raghothama K.G., Baek D., Koo Y.D., Jin J.B., Bressan R.A., et al. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102 (2005) 7760-7765. In this study, the authors identify that AtSIZ1 is a SUMO E3 ligase. The mutation in AtSIZ1 caused hyper-response to phosphate deficiency, including cessation of primary root growth, enhanced lateral root and root hair development, and increased anthocyanin accumulation. The work reveals that the MYB transcription factor PHR1 is one of sumoylation target proteins.
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Proc Natl Acad Sci USA
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Miura, K.1
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33845630288
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SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid
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The work described in this paper reveals that AtSIZ1 positively regulates basal, not required, thermotolerance. Because reduction of hyperaccumulation of salicylic acid in siz1 by NahG still leads to increase in thermosensitivity, this regulation is independent of salicylic acid signaling.
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Yoo C.Y., Miura K., Jin J.B., Lee J., Park H.C., Salt D.E., Yun D.-J., Bressan R.A., and Hasegawa P.M. SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142 (2006) 1548-1558. The work described in this paper reveals that AtSIZ1 positively regulates basal, not required, thermotolerance. Because reduction of hyperaccumulation of salicylic acid in siz1 by NahG still leads to increase in thermosensitivity, this regulation is independent of salicylic acid signaling.
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Plant Physiol
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Yoo, C.Y.1
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Yun, D.-J.7
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Hasegawa, P.M.9
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19
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SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis
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In this paper, the authors report that the siz1 mutation caused freezing and chilling sensitivity because of repression of CBF/DREB1s and their regulon gene expression. In vitro and in vivo assay revealed that the MYC-like transcription factor ICE1 (inducer of CBF expression) was sumoylated at K393 to activate and/or stabilize ICE1. The substitution of K393 to R repressed CBF3/DREB1A and its regulon gene expression and decreased freezing tolerance.
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Miura K., Jin J.B., Lee J., Yoo C.Y., Stirm V., Miura T., Ashworth E.N., Bressan R.A., Yun D.-J., and Hasegawa P.M. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19 (2007) 1403-1414. In this paper, the authors report that the siz1 mutation caused freezing and chilling sensitivity because of repression of CBF/DREB1s and their regulon gene expression. In vitro and in vivo assay revealed that the MYC-like transcription factor ICE1 (inducer of CBF expression) was sumoylated at K393 to activate and/or stabilize ICE1. The substitution of K393 to R repressed CBF3/DREB1A and its regulon gene expression and decreased freezing tolerance.
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Plant Cell
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Miura, K.1
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Ashworth, E.N.7
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Bossis G., and Melchior F. SUMO: regulating the regulator. Cell Div 1 (2006) 13
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Heun P. SUMOrganization of the nucleus. Curr Opin Cell Biol 19 (2007) 1-6
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Novatchkova M., Budhiraja R., Coupland G., Eisenhaber F., and Bachmair A. SUMO conjugation in plants. Planta 220 (2004) 1-8
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Murtas G., Reeves P.H., Fu Y.-F., Bancroft I., Dean C., and Coupland G. A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15 (2003) 2308-2319
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In this paper, biochemical analyses revealed that Arabidopsis sumoylation components have conjugation and deconjugation activity. AtSUMO1, 2, and 3 conjugated to ScPCNA (a yeast substrate) by using AtSAE1, AtSAE2, and AtSCE1 recombinant proteins. The conjugation was dissociated by AtULP1C, AtULP1D, and AtESD4.
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Colby T., Matthäi A., Boeckelmann A., and Stuible H.-P. SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol 142 (2006) 318-332. In this paper, biochemical analyses revealed that Arabidopsis sumoylation components have conjugation and deconjugation activity. AtSUMO1, 2, and 3 conjugated to ScPCNA (a yeast substrate) by using AtSAE1, AtSAE2, and AtSCE1 recombinant proteins. The conjugation was dissociated by AtULP1C, AtULP1D, and AtESD4.
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In this paper, the authors identify ULP1 family SUMO proteases in Arabidopsis. The catalytic domain of ULP1s show high similarity with each other and yeast Ulp1, but N-terminal region of these proteases share limited sequence identity. The N-terminal region plays a key role in not only modulating the enzyme activity but also in specifying SUMO proteins.
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Chosed R., Mukherjee S., Lois L.M., and Orth K. Evolution of a signalling system that incorporates both redundancy and diversity: Arabidopsis SUMOylation. Biochem J 398 (2006) 521-529. In this paper, the authors identify ULP1 family SUMO proteases in Arabidopsis. The catalytic domain of ULP1s show high similarity with each other and yeast Ulp1, but N-terminal region of these proteases share limited sequence identity. The N-terminal region plays a key role in not only modulating the enzyme activity but also in specifying SUMO proteins.
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Lois L.M., and Lima D.C. Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J 24 (2005) 439-451
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Sharrocks A.D. PIAS proteins and transcriptional regulation - more than just SUMO E3 ligases?. Genes Dev 20 (2006) 754-758. This is a recent review that describes two distinct functions of PIAS proteins, SUMO E3 ligase activity and regulation of other proteins in a SUMO E3-independent manner.
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Takahashi Y., and Kikuchi S. Yeast PIAS-type Ull1/Siz1 is composed of SUMO ligase and regulatory domains. J Biol Chem 280 (2005) 35822-35828
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Gross M., Yang R., Top I., Gasper C., and Shuai K. PIASy-mediated repression of the androgen receptor is independent of sumoylation. Oncogene 23 (2004) 3059-3066
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Gozani O., Karuman P., Jones D.R., Ivanov D., Cha J., Lugovskoy A.A., Baird C.L., Zhu H., Field S.J., Lessnick S.L., et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114 (2003) 99-111
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Potts P.R., and Yu H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol Cell Biol 25 (2005) 7021-7032
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In this paper, authors report that NUA, nuclear pore anchor, is a 237-kDa protein, which interacts with AtESD4 at nuclear envelope to regulate desumoylation activity of the SUMO protease. The nua mutation increased SUMO-conjugates and promoted early flowering as did the esd4 mutation.
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Xu X.M., Rose A., Muthuswamy S., Jeong S.Y., Venkatakrishnan S., Zhao Q., and Meier I. NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/Megator, is involve in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19 (2007) 1537-1548. In this paper, authors report that NUA, nuclear pore anchor, is a 237-kDa protein, which interacts with AtESD4 at nuclear envelope to regulate desumoylation activity of the SUMO protease. The nua mutation increased SUMO-conjugates and promoted early flowering as did the esd4 mutation.
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Xu, X.M.1
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Hilgarth R.S., Murphy L.A., O'Connor C.M., Clark J.A., Park-Sarge O.K., and Sarge K.D. Identification of Xenopus heat shock transcription factor-2: conserved role of sumoylation in regulating deoxyribonucleic acid-binding activity of heat shock transcription factor-2 proteins. Cell Stress Chaperones 9 (2004) 214-220
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The work reveals that siz1 mutant plants exhibited constitutive systemic-acquired resistance characterized by hyperaccumulation of SA, constitutive expression of pathogenesis-related genes, and increased resistance to bacteria pathogen Pseudomonas syringae pv. tomato DC3000. Because pad4 is epistatic to siz1, SIZ1 negatively controls PAD4-mediated TIR-NBS-LRR-type R gene signaling. However, SIZ1 is not involved in jasmonic acid signaling or defense against Botrytis cinerea.
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Lee J., Nam J., Park H.C., Na G., Miura K., Jin J.B., Yoo C.Y., Baek D., Kim D.H., Jeoung J.C., et al. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49 (2007) 79-90. The work reveals that siz1 mutant plants exhibited constitutive systemic-acquired resistance characterized by hyperaccumulation of SA, constitutive expression of pathogenesis-related genes, and increased resistance to bacteria pathogen Pseudomonas syringae pv. tomato DC3000. Because pad4 is epistatic to siz1, SIZ1 negatively controls PAD4-mediated TIR-NBS-LRR-type R gene signaling. However, SIZ1 is not involved in jasmonic acid signaling or defense against Botrytis cinerea.
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In this paper, the authors identified the contact residues between plant SUMOs and the SUMO protease XopD, a type III secretion system effector in Xanthomonas. These residues are different from those of yeast SUMO. Because XopD only recognizes plant SUMOs, this difference contributes to the specificity of XopD.
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Chosed R., Tomchick D.R., Brautigam C.A., Mukherjee S., Negi V.S., Machius M., and Orth K. Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitin-like protein proteases. J Biol Chem 282 (2007) 6773-6782. In this paper, the authors identified the contact residues between plant SUMOs and the SUMO protease XopD, a type III secretion system effector in Xanthomonas. These residues are different from those of yeast SUMO. Because XopD only recognizes plant SUMOs, this difference contributes to the specificity of XopD.
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Deslandes L., Olivier J., Peeters N., Feng D.X., Khounlotham M., Boucher C., Somssich I., Genin S., and Marcho Y. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA 100 (2003) 8024-8029
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Reeves P.H., Murtas G., Dash S., and Coupland G. Early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC. Development 129 (2002) 5349-5361
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