Home LiteratureArticle Details
PMID: 22814374 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 109 ·No. 31 ·2012-07-31 ·Pages 12822-7

Zheng Y, Schumaker KS, Guo Y

Abstract

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.

MeSH Terms
Abscisic Acid/genetics,metabolism Amino Acid Substitution Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Basic-Leucine Zipper Transcription Factors/genetics,metabolism Gene Expression Regulation, Plant/physiology Germination/physiology Ligases/genetics,metabolism Mutation, Missense Seeds/genetics,metabolism Signal Transduction/physiology Sumoylation/physiology Transcription Factors/genetics,metabolism Ubiquitin-Protein Ligases/genetics,metabolism
Chemicals
ABI5 protein, Arabidopsis Arabidopsis Proteins Basic-Leucine Zipper Transcription Factors MYB30 protein, Arabidopsis Transcription Factors Abscisic Acid Ubiquitin-Protein Ligases Ligases SIZ1 protein, Arabidopsis
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zheng Yuan
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100094, China.
Schumaker Karen S
Guo Yan
References (49)
49 references, click to expand
  1. ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana.
    J Biol Chem. 2001 Nov 2;276(44):40381-4 PMID: 11553608
  2. ABA receptors: the START of a new paradigm in phytohormone signalling.
    J Exp Bot. 2010 Jul;61(12):3199-210 PMID: 20522527
  3. Sumoylation and other ubiquitin-like post-translational modifications in plants.
    Trends Cell Biol. 2010 Apr;20(4):223-32 PMID: 20189809
  4. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression.
    Plant Cell. 2001 Sep;13(9):2063-83 PMID: 11549764
  5. A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis.
    Plant Cell. 2008 Mar;20(3):752-67 PMID: 18326828
  6. Flowering time regulation by the SUMO E3 ligase SIZ1.
    Plant Signal Behav. 2008 Oct;3(10):891-2 PMID: 19704532
  7. Reconstitution of Arabidopsis thaliana SUMO pathways in E. coli: functional evaluation of SUMO machinery proteins and mapping of SUMOylation sites by mass spectrometry.
    Plant Cell Physiol. 2009 Jun;50(6):1049-61 PMID: 19376783
  8. The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response.
    Plant Physiol. 2011 Jun;156(2):550-63 PMID: 21478367
  9. SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid.
    Plant Physiol. 2006 Dec;142(4):1548-58 PMID: 17041025
  10. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17588-93 PMID: 19805022
  11. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
    Science. 2009 May 22;324(5930):1068-71 PMID: 19407142
  12. Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1.
    Plant Physiol. 2006 Aug;141(4):1389-99 PMID: 16798945
  13. Signaling pathways mediating the suppression of Arabidopsis thaliana Ku gene expression by abscisic acid.
    Biochim Biophys Acta. 2008 Mar;1779(3):164-74 PMID: 18179780
  14. Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression.
    Plant J. 2009 Apr;58(2):275-86 PMID: 19170933
  15. Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis.
    J Biol Chem. 2002 Mar 8;277(10):8588-96 PMID: 11779861
  16. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions.
    Plant Cell. 2002 Nov;14(11):2723-43 PMID: 12417697
  17. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde.
    Plant Cell. 2002 Aug;14(8):1833-46 PMID: 12172025
  18. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid.
    Cell. 2006 Sep 22;126(6):1109-20 PMID: 16990135
  19. Sumoylation, a post-translational regulatory process in plants.
    Curr Opin Plant Biol. 2007 Oct;10(5):495-502 PMID: 17720613
  20. SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid.
    Plant Cell Physiol. 2010 Jan;51(1):103-13 PMID: 20007967
  21. A novel myb oncogene homologue in Arabidopsis thaliana related to hypersensitive cell death.
    Plant J. 1999 Oct;20(1):57-66 PMID: 10571865
  22. Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling.
    Plant Physiol. 2009 Nov;151(3):1339-53 PMID: 19726569
  23. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4782-7 PMID: 11287670
  24. Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression.
    Plant Cell Physiol. 2010 May;51(5):842-7 PMID: 20375108
  25. SUMO: a history of modification.
    Mol Cell. 2005 Apr 1;18(1):1-12 PMID: 15808504
  26. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy.
    Plant Cell Physiol. 2009 Jul;50(7):1345-63 PMID: 19541597
  27. Modification with SUMO. A role in transcriptional regulation.
    EMBO Rep. 2003 Feb;4(2):137-42 PMID: 12612601
  28. KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling.
    Plant Cell. 2006 Dec;18(12):3415-28 PMID: 17194765
  29. PvALF and FUS3 activate expression from the phaseolin promoter by different mechanisms.
    Plant Mol Biol. 2008 Feb;66(3):233-44 PMID: 18038114
  30. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo.
    Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1717-22 PMID: 21220313
  31. Regulators of PP2C phosphatase activity function as abscisic acid sensors.
    Science. 2009 May 22;324(5930):1064-8 PMID: 19407143
  32. An essential role for salicylic acid in AtMYB30-mediated control of the hypersensitive cell death program in Arabidopsis.
    FEBS Lett. 2006 Jun 12;580(14):3498-504 PMID: 16730712
  33. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis.
    Plant Cell. 2007 Apr;19(4):1403-14 PMID: 17416732
  34. The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense.
    Plant Cell. 2011 Sep;23(9):3498-511 PMID: 21917550
  35. A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid.
    Science. 2007 Mar 23;315(5819):1712-6 PMID: 17347412
  36. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing.
    EMBO Rep. 2008 Mar;9(3):273-9 PMID: 18259216
  37. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation.
    Genes Dev. 2003 Feb 1;17(3):410-8 PMID: 12569131
  38. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism.
    EMBO J. 2004 Apr 7;23(7):1647-56 PMID: 15044947
  39. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis.
    Cell. 2009 Jan 9;136(1):136-48 PMID: 19135895
  40. Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling.
    Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5418-23 PMID: 19276109
  41. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase.
    Plant J. 2007 Jan;49(1):79-90 PMID: 17163880
  42. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis.
    Plant Cell. 2007 Feb;19(2):485-94 PMID: 17307925
  43. Structural and functional insights into core ABA signaling.
    Curr Opin Plant Biol. 2010 Oct;13(5):495-502 PMID: 20934900
  44. A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):10179-84 PMID: 12119395
  45. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses.
    Proc Natl Acad Sci U S A. 2005 May 24;102(21):7760-5 PMID: 15894620
  46. The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses.
    Plant Cell. 2007 Sep;19(9):2952-66 PMID: 17905899
  47. The Mg-chelatase H subunit is an abscisic acid receptor.
    Nature. 2006 Oct 19;443(7113):823-6 PMID: 17051210
  48. AtsPLA2-alpha nuclear relocalization by the Arabidopsis transcription factor AtMYB30 leads to repression of the plant defense response.
    Proc Natl Acad Sci U S A. 2010 Aug 24;107(34):15281-6 PMID: 20696912
  49. The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure.
    Plant J. 2008 Feb;53(3):530-40 PMID: 18069938
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.1202630109
Published
2012-07-31
Epub
2012-00-18
Pages
12822-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3411956
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.1202630109 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2