Home LiteratureArticle Details
PMID: 15377756 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity.

The Plant cell ·Vol. 16 ·No. 10 ·2004-10-00 ·Pages 2795-808

Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL

Abstract

The rice (Oryza sativa) spotted leaf11 (spl11) mutant was identified from an ethyl methanesulfonate-mutagenized indica cultivar IR68 population and was previously shown to display a spontaneous cell death phenotype and enhanced resistance to rice fungal and bacterial pathogens. Here, we have isolated Spl11 via a map-based cloning strategy. The isolation of the Spl11 gene was facilitated by the identification of three additional spl11 alleles from an IR64 mutant collection. The predicted SPL11 protein contains both a U-box domain and an armadillo (ARM) repeat domain, which were demonstrated in yeast and mammalian systems to be involved in ubiquitination and protein-protein interactions, respectively. Amino acid sequence comparison indicated that the similarity between SPL11 and other plant U-box-ARM proteins is mostly restricted to the U-box and ARM repeat regions. A single base substitution was detected in spl11, which results in a premature stop codon in the SPL11 protein. Expression analysis indicated that Spl11 is induced in both incompatible and compatible rice-blast interactions. In vitro ubiquitination assay indicated that the SPL11 protein possesses E3 ubiquitin ligase activity that is dependent on an intact U-box domain, suggesting a role of the ubiquitination system in the control of plant cell death and defense.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Cell Death/physiology Chromosomes, Plant DNA Primers Drosophila melanogaster Genetic Complementation Test Molecular Sequence Data Mutation Oryza Physical Chromosome Mapping Plant Proteins/chemistry,genetics,physiology Reverse Transcriptase Polymerase Chain Reaction Sequence Homology, Amino Acid Ubiquitin-Protein Ligases/metabolism
Chemicals
DNA Primers Plant Proteins Ubiquitin-Protein Ligases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zeng Li-Rong
Department of Plant Pathology, Ohio State University, Columbus, Ohio 43210, USA.
Qu Shaohong
Bordeos Alicia
Yang Chengwei
Baraoidan Marietta
Yan Hongyan
Xie Qi
Nahm Baek Hie
Leung Hei
Wang Guo-Liang
References (52)
52 references, click to expand
  1. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype.
    Mol Gen Genet. 1993 May;239(1-2):122-8 PMID: 8510641
  2. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly.
    Cell. 1999 Mar 5;96(5):635-44 PMID: 10089879
  3. The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis.
    Nat Cell Biol. 2002 Jun;4(6):445-50 PMID: 12021771
  4. U box proteins as a new family of ubiquitin-protein ligases.
    J Biol Chem. 2001 Aug 31;276(35):33111-20 PMID: 11435423
  5. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family.
    Plant Cell. 2003 Feb;15(2):365-79 PMID: 12566578
  6. The diverse roles of ubiquitin and the 26S proteasome in the life of plants.
    Nat Rev Genet. 2003 Dec;4(12):948-58 PMID: 14631355
  7. Characterization of interactions among the Cef1p-Prp19p-associated splicing complex.
    RNA. 2002 Jun;8(6):798-815 PMID: 12088152
  8. CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco.
    Biochim Biophys Acta. 2003 Sep 23;1651(1-2):50-9 PMID: 14499588
  9. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death.
    Cell. 1997 Mar 7;88(5):685-94 PMID: 9054508
  10. The barley Mlo gene: a novel control element of plant pathogen resistance.
    Cell. 1997 Mar 7;88(5):695-705 PMID: 9054509
  11. Developmental programmed cell death in plants.
    Curr Opin Plant Biol. 2002 Dec;5(6):568-73 PMID: 12393021
  12. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics.
    Br J Cancer. 1972 Aug;26(4):239-57 PMID: 4561027
  13. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis.
    Plant Cell. 2001 Oct;13(10):2211-24 PMID: 11595797
  14. Role of ubiquitination in the regulation of plant defence against pathogens.
    Curr Opin Plant Biol. 2003 Aug;6(4):307-11 PMID: 12873523
  15. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize.
    Cell. 1997 Apr 4;89(1):25-31 PMID: 9094711
  16. A fatty acid desaturase modulates the activation of defense signaling pathways in plants.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9448-53 PMID: 11481500
  17. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles.
    Plant Cell. 2000 Jun;12(6):963-77 PMID: 10852940
  18. A novel HECT-type E3 ubiquitin ligase, NEDL2, stabilizes p73 and enhances its transcriptional activity.
    Biochem Biophys Res Commun. 2003 Aug 15;308(1):106-13 PMID: 12890487
  19. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation.
    J Biol Chem. 2001 Nov 16;276(46):42938-44 PMID: 11557750
  20. EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b.
    Plant J. 2002 May;30(4):447-55 PMID: 12028574
  21. Three-dimensional structure of the armadillo repeat region of beta-catenin.
    Cell. 1997 Sep 5;90(5):871-82 PMID: 9298899
  22. Drosophila Morgue is an F box/ubiquitin conjugase domain protein important for grim-reaper mediated apoptosis.
    Nat Cell Biol. 2002 Jun;4(6):451-6 PMID: 12021772
  23. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  24. The U box is a modified RING finger - a common domain in ubiquitination.
    Curr Biol. 2000 Feb 24;10(4):R132-4 PMID: 10704423
  25. The U-box protein family in plants.
    Trends Plant Sci. 2001 Aug;6(8):354-8 PMID: 11495788
  26. Two broad-spectrum blast resistance genes, Pi9( t) and Pi2( t), are physically linked on rice chromosome 6.
    Mol Genet Genomics. 2002 Jun;267(4):472-80 PMID: 12111554
  27. Cell death in development.
    Cell. 1999 Jan 22;96(2):245-54 PMID: 9988219
  28. Lesion mimic mutants of rice with alterations in early signaling events of defense.
    Plant J. 1999 Mar;17(5):535-45 PMID: 10205906
  29. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals.
    Nature. 2002 Sep 12;419(6903):167-70 PMID: 12226665
  30. A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family.
    Plant Physiol. 2004 Jan;134(1):59-66 PMID: 14657406
  31. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen.
    Plant Cell. 2003 Apr;15(4):885-98 PMID: 12671085
  32. Regulation of apoptosis by ubiquitination.
    Immunol Rev. 2003 Jun;193:39-47 PMID: 12752669
  33. Identification of human gene structure using linear discriminant functions and dynamic programming.
    Proc Int Conf Intell Syst Mol Biol. 1995;3:367-75 PMID: 7584460
  34. Prediction of complete gene structures in human genomic DNA.
    J Mol Biol. 1997 Apr 25;268(1):78-94 PMID: 9149143
  35. Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo.
    Cell. 2001 Aug 10;106(3):343-54 PMID: 11509183
  36. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight.
    Mol Plant Microbe Interact. 2000 Aug;13(8):869-76 PMID: 10939258
  37. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae.
    Plant Cell. 2003 Feb;15(2):317-30 PMID: 12566575
  38. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize.
    Plant Cell. 1998 Jul;10(7):1095-1105 PMID: 9668130
  39. PROGRAMMED CELL DEATH IN PLANT-PATHOGEN INTERACTIONS.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:525-545 PMID: 15012273
  40. A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum.
    Plant J. 2001 Apr;26(2):217-27 PMID: 11389762
  41. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?
    Trends Plant Sci. 2003 Jun;8(6):263-71 PMID: 12818660
  42. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling.
    Electrophoresis. 1997 Dec;18(15):2714-23 PMID: 9504803
  43. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  44. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.
    Science. 2002 Mar 15;295(5562):2073-6 PMID: 11847307
  45. Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene.
    Genes Dev. 1989 Jan;3(1):96-113 PMID: 2707602
  46. Direct delivery of bacterial avirulence proteins into resistant Arabidopsis protoplasts leads to hypersensitive cell death.
    Plant J. 2003 Jan;33(1):131-7 PMID: 12943547
  47. Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense.
    Genes Dev. 2002 Feb 15;16(4):490-502 PMID: 11850411
  48. Structural insights into the U-box, a domain associated with multi-ubiquitination.
    Nat Struct Biol. 2003 Apr;10(4):250-5 PMID: 12627222
  49. A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7530-5 PMID: 12032317
  50. A repeating amino acid motif shared by proteins with diverse cellular roles.
    Cell. 1994 Mar 11;76(5):789-91 PMID: 7907279
  51. Fine genetic mapping and physical delimitation of the lesion mimic gene Spl11 to a 160-kb DNA segment of the rice genome.
    Mol Genet Genomics. 2002 Oct;268(2):253-61 PMID: 12395200
  52. Identification and mapping of polymorphisms in cereals based on the polymerase chain reaction.
    Theor Appl Genet. 1991 Aug;82(2):209-16 PMID: 24213068
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.104.025171
Published
2004-10-00
Epub
2004-00-17
Pages
2795-808
Language
English
Region
England
NLM ID
9208688
PMCID
PMC520972
Subset
IM
Databases
GENBANK
AY652589, AY652590
External Links
PubMed source DOI: 10.1105/tpc.104.025171 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: [email protected]

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