Home LiteratureArticle Details
PMID: 21772271 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1.

Nature communications ·Vol. 2 ·2011-07-19 ·Pages 400

Park BS, Song JT, Seo HS

Abstract

Small ubiquitin-related modifier (SUMO) is a small polypeptide that modulates protein activity and regulates hormone signalling, abiotic and biotic responses in plants. Here we show that AtSIZ regulates nitrogen assimilation in Arabidopsis through its E3 SUMO ligase function. Dwarf plants of siz1-2 flower early, show abnormal seed development and have high salicylic acid content and enhanced resistance to bacterial pathogens. These mutant phenotypes are reverted to wild-type phenotypes by exogenous ammonium but not by nitrate, phosphate or potassium. Decreased nitrate reductase activity in siz1-2 plants resulted in low nitrogen concentrations, low nitric oxide production and high nitrate content in comparison with wild-type plants. The nitrate reductases, NIA1 and NIA2, are sumoylated by AtSIZ1, which dramatically increases their activity. Both sumoylated and non-sumoylated NIA1 and NIA2 can form dimers. Our results indicate that AtSIZ1 positively controls nitrogen assimilation by promoting sumoylation of NRs in Arabidopsis.

MeSH Terms
Arabidopsis/enzymology,immunology,metabolism,microbiology Arabidopsis Proteins/genetics,metabolism Colony Count, Microbial Ligases/genetics,metabolism Mutation/genetics Nitrate Reductase/chemistry,metabolism Nitrates/analysis Nitric Oxide/biosynthesis Protein Multimerization Pseudomonas syringae/immunology Quaternary Ammonium Compounds/pharmacology Salicylic Acid/analysis Seeds/chemistry Small Ubiquitin-Related Modifier Proteins/metabolism Sumoylation Ubiquitin-Protein Ligases/metabolism
Chemicals
Arabidopsis Proteins Nitrates Quaternary Ammonium Compounds Small Ubiquitin-Related Modifier Proteins Nitric Oxide Nitrate Reductase Ubiquitin-Protein Ligases Ligases SIZ1 protein, Arabidopsis Salicylic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Park Bong Soo
Department of Plant Science, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea.
Song Jong Tae
Seo Hak Soo
References (53)
53 references, click to expand
  1. 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
  2. 14-3-3 proteins control proteolysis of nitrate reductase in spinach leaves.
    FEBS Lett. 1999 Jul 16;455(1-2):75-8 PMID: 10428475
  3. Preparation of sumoylated substrates for biochemical analysis.
    Methods Mol Biol. 2009;497:201-10 PMID: 19107419
  4. Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in constitutive activation of the enzyme in vivo and nitrite accumulation.
    Plant J. 2003 Sep;35(5):566-73 PMID: 12940950
  5. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress.
    Plant J. 2003 Sep;35(6):763-70 PMID: 12969429
  6. SUMOylation attenuates the function of PGC-1alpha.
    J Biol Chem. 2009 Sep 18;284(38):26184-93 PMID: 19625249
  7. Sumo-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor.
    J Biol Chem. 2001 May 25;276(21):18513-8 PMID: 11278381
  8. Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential.
    Plant Physiol. 2007 Sep;145(1):119-34 PMID: 17644626
  9. Nitrogen Utilization in Lemna: II. Studies of Nitrate Uptake Using NO(3).
    Plant Physiol. 1987 Nov;85(3):860-4 PMID: 16665791
  10. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis.
    Plant Cell. 2007 Apr;19(4):1403-14 PMID: 17416732
  11. SUMOylation enhances DNA methyltransferase 1 activity.
    Biochem J. 2009 Jul 15;421(3):449-61 PMID: 19450230
  12. 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
  13. Adenosine signaling mediates SUMO-1 modification of IkappaBalpha during hypoxia and reoxygenation.
    J Biol Chem. 2009 May 15;284(20):13686-13695 PMID: 19297320
  14. Covalent attachment of the SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity.
    J Biol Chem. 2002 Mar 15;277(11):8999-9009 PMID: 11779867
  15. Differential expression of the arabidopsis nia1 and nia2 genes. cytokinin-induced nitrate reductase activity is correlated with increased nia1 transcription and mrna levels
    Plant Physiol. 1998 Mar;116(3):1091-6 PMID: 9501142
  16. Markers and signals associated with nitrogen assimilation in higher plants.
    J Exp Bot. 2003 Jan;54(382):585-93 PMID: 12508069
  17. Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue.
    Planta. 2004 May;219(1):59-65 PMID: 14767769
  18. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization.
    Mol Cell. 2002 Oct;10(4):831-42 PMID: 12419227
  19. Sumoylation and other ubiquitin-like post-translational modifications in plants.
    Trends Cell Biol. 2010 Apr;20(4):223-32 PMID: 20189809
  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. Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes.
    Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17415-20 PMID: 20855607
  22. Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1).
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14145-50 PMID: 11121022
  23. Functional domains of assimilatory nitrate reductases and nitrite reductases.
    Trends Biochem Sci. 1990 Aug;15(8):315-9 PMID: 2204158
  24. Steps towards an integrated view of nitrogen metabolism.
    J Exp Bot. 2002 Apr;53(370):959-70 PMID: 11912238
  25. A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates.
    Plant Cell. 2003 Oct;15(10):2308-19 PMID: 14507998
  26. Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis.
    Plant Cell. 2003 Jun;15(6):1347-59 PMID: 12782728
  27. SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis.
    Plant Physiol. 2006 Sep;142(1):318-32 PMID: 16920872
  28. Nucleotide sequence of a gene for nitrite reductase from Arabidopsis thaliana.
    DNA Seq. 1994;5(1):57-61 PMID: 7894060
  29. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation.
    Plant J. 2007 Apr;50(2):320-37 PMID: 17355433
  30. The Conversion of Nitrite to Nitrogen Oxide(s) by the Constitutive NAD(P)H-Nitrate Reductase Enzyme from Soybean.
    Plant Physiol. 1988 Oct;88(2):389-95 PMID: 16666314
  31. Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots.
    J Plant Physiol. 2010 Jan 1;167(1):77-80 PMID: 19822377
  32. Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants.
    Plant Cell Physiol. 2008 Jul;49(7):1112-21 PMID: 18540030
  33. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta.
    Mol Microbiol. 2003 Oct;50(2):377-89 PMID: 14617166
  34. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana.
    Plant J. 2009 Jul;59(2):316-28 PMID: 19302419
  35. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16314-8 PMID: 12446847
  36. SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation.
    J Plant Physiol. 2010 May 1;167(7):555-60 PMID: 19959255
  37. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis.
    Plant Physiol. 2004 Sep;136(1):2512-22 PMID: 15333754
  38. Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification.
    J Biol Chem. 2001 Oct 26;276(43):40263-7 PMID: 11514557
  39. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro.
    J Exp Bot. 2002 Jan;53(366):103-10 PMID: 11741046
  40. Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and -2 regulate salt stress responses in Arabidopsis.
    Plant Cell. 2008 Oct;20(10):2894-908 PMID: 18849491
  41. Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis.
    Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16512-7 PMID: 20813957
  42. Regulation of protein tyrosine phosphatase 1B by sumoylation.
    Nat Cell Biol. 2007 Jan;9(1):80-5 PMID: 17159996
  43. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase.
    Plant J. 2007 Jan;49(1):79-90 PMID: 17163880
  44. Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system.
    Mol Plant Microbe Interact. 2001 Feb;14(2):145-55 PMID: 11204777
  45. Nitric oxide represses the Arabidopsis floral transition.
    Science. 2004 Sep 24;305(5692):1968-71 PMID: 15448272
  46. 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
  47. The PHD domain of plant PIAS proteins mediates sumoylation of bromodomain GTE proteins.
    J Biol Chem. 2008 Aug 1;283(31):21469-77 PMID: 18502747
  48. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress.
    J Biol Chem. 2003 Feb 28;278(9):6862-72 PMID: 12482876
  49. Local and long-range signaling pathways regulating plant responses to nitrate.
    Annu Rev Plant Biol. 2002;53:203-24 PMID: 12221973
  50. Mechanisms, regulation and consequences of protein SUMOylation.
    Biochem J. 2010 May 13;428(2):133-45 PMID: 20462400
  51. The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses.
    Plant Cell. 2007 Sep;19(9):2952-66 PMID: 17905899
  52. Regulation of plant NR activity by reversible phosphorylation, 14-3-3 proteins and proteolysis.
    Cell Mol Life Sci. 2001 Feb;58(2):205-14 PMID: 11289302
  53. 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
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
Published
2011-07-19
Epub
2011-00-19
Pages
400
Language
English
Region
England
NLM ID
101528555
PMCID
PMC3160146
Subset
IM
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: [email protected]