Home LiteratureArticle Details
PMID: 16169895 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis.

The Plant cell ·Vol. 17 ·No. 10 ·2005-10-00 ·Pages 2723-37

Brukhin V, Gheyselinck J, Gagliardini V, Genschik P, Grossniklaus U

Abstract

The 26S proteasome plays a central role in the degradation of regulatory proteins involved in a variety of developmental processes. It consists of two multisubunit protein complexes: the proteolytic core protease and the regulatory particle (RP). The function of most RP subunits is poorly understood. Here, we describe mutants in the Arabidopsis thaliana RPN1 subunit, which is encoded by two paralogous genes, RPN1a and RPN1b. Disruption of RPN1a caused embryo lethality, while RPN1b mutants showed no obvious abnormal phenotype. Embryos homozygous for rpn1a arrested at the globular stage with defects in the formation of the embryonic root, the protoderm, and procambium. Cyclin B1 protein was not degraded in these embryos, consistent with cell division defects. Double mutant plants (rpn1a/RPN1a rpn1b/rpn1b) produced embryos with a phenotype indistinguishable from that of the rpn1a single mutant. Thus, despite their largely overlapping expression patterns in flowers and developing seeds, the two isoforms do not share redundant functions during gametogenesis and embryogenesis. However, complementation of the rpn1a mutation with the coding region of RPN1b expressed under the control of the RPN1a promoter indicates that the two RPN1 isoforms are functionally equivalent. Overall, our data indicate that RPN1 activity is essential during embryogenesis, where it might participate in the destruction of a specific set of protein substrates.

MeSH Terms
Arabidopsis/embryology,genetics,metabolism Arabidopsis Proteins/genetics,metabolism Cell Division/genetics Cyclin B/genetics,metabolism Cyclin B1 Embryonic Development/genetics Gametogenesis/genetics Gene Expression Regulation, Plant/genetics Genes, Lethal/genetics Mutation/genetics Phenotype Proteasome Endopeptidase Complex/genetics,metabolism Protein Isoforms/genetics,metabolism Protein Subunits/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Seeds/genetics,metabolism
Chemicals
Arabidopsis Proteins Cyclin B Cyclin B1 Protein Isoforms Protein Subunits RPN1 protein, Arabidopsis RPN1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Proteasome Endopeptidase Complex ATP dependent 26S protease
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Brukhin Vladimir
Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, CH-8008 Zürich, Switzerland.
Gheyselinck Jacqueline
Gagliardini Valeria
Genschik Pascal
Grossniklaus Ueli
References (72)
72 references, click to expand
  1. The 26S proteasome: a molecular machine designed for controlled proteolysis.
    Annu Rev Biochem. 1999;68:1015-68 PMID: 10872471
  2. Ubiquitin-mediated proteolysis: biological regulation via destruction.
    Bioessays. 2000 May;22(5):442-51 PMID: 10797484
  3. Mitosis in plants: how far we have come at the molecular level?
    Curr Opin Plant Biol. 2002 Dec;5(6):487-93 PMID: 12393010
  4. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins.
    Trends Plant Sci. 2003 Mar;8(3):135-42 PMID: 12663224
  5. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development.
    EMBO J. 1998 Mar 2;17(5):1405-11 PMID: 9482737
  6. Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia.
    Plant Cell. 1999 May;11(5):793-808 PMID: 10330466
  7. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  8. The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana.
    Plant J. 2001 Sep;27(5):393-405 PMID: 11576424
  9. Conservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopsis thaliana.
    Plant Mol Biol. 2003 Sep;53(1-2):163-73 PMID: 14756314
  10. Back to the future with ubiquitin.
    Cell. 2004 Jan 23;116(2):181-90 PMID: 14744430
  11. Analysis of flanking sequences from dissociation insertion lines: a database for reverse genetics in Arabidopsis.
    Plant Cell. 1999 Dec;11(12):2263-70 PMID: 10590156
  12. The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1.
    Genes Dev. 2003 Jun 15;17(12):1540-53 PMID: 12815071
  13. A proteolytic system that compensates for loss of proteasome function.
    Nature. 1998 Apr 9;392(6676):618-22 PMID: 9560160
  14. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome.
    EMBO J. 2001 Dec 17;20(24):7096-107 PMID: 11742986
  15. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity.
    Genes Dev. 1999 Nov 15;13(22):2971-82 PMID: 10580004
  16. Getting in and out of the proteasome.
    Semin Cell Dev Biol. 2000 Jun;11(3):149-58 PMID: 10906271
  17. Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome.
    J Biol Chem. 2004 Jun 25;279(26):26817-22 PMID: 15117949
  18. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  19. Proteasome subunit Rpn1 binds ubiquitin-like protein domains.
    Nat Cell Biol. 2002 Sep;4(9):725-30 PMID: 12198498
  20. Functional characterization of rpn3 uncovers a distinct 19S proteasomal subunit requirement for ubiquitin-dependent proteolysis of cell cycle regulatory proteins in budding yeast.
    Mol Cell Biol. 1999 Oct;19(10):6872-90 PMID: 10490625
  21. FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis.
    Genes Dev. 2000 Jun 15;14(12):1471-84 PMID: 10859166
  22. The Arabidopsis 1-Aminocyclopropane-1-Carboxylate Synthase Gene 1 Is Expressed during Early Development.
    Plant Cell. 1993 Aug;5(8):897-911 PMID: 12271088
  23. Themes and variations on ubiquitylation.
    Nat Rev Mol Cell Biol. 2001 Mar;2(3):169-78 PMID: 11265246
  24. The 26S proteasome of the fission yeast Schizosaccharomyces pombe.
    Philos Trans R Soc Lond B Biol Sci. 1999 Sep 29;354(1389):1523-32 PMID: 10582238
  25. Cell cycling and cell enlargement in developing leaves of Arabidopsis.
    Dev Biol. 1999 Nov 15;215(2):407-19 PMID: 10545247
  26. The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit.
    Plant Cell. 2003 Oct;15(10):2370-82 PMID: 14508008
  27. Plant development: regulation by protein degradation.
    Science. 2002 Aug 2;297(5582):793-7 PMID: 12161644
  28. A HECT domain E3 enzyme assembles novel polyubiquitin chains.
    J Biol Chem. 2001 Jun 8;276(23):19871-8 PMID: 11278995
  29. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome.
    Genome Res. 2003 Feb;13(2):137-44 PMID: 12566392
  30. The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover.
    Mol Cell Biol. 1996 Nov;16(11):6020-8 PMID: 8887631
  31. The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis.
    Plant J. 2003 Dec;36(6):853-66 PMID: 14675450
  32. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis.
    Genetics. 1998 Jun;149(2):621-31 PMID: 9611178
  33. Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover.
    Nat Rev Mol Cell Biol. 2003 Nov;4(11):855-64 PMID: 14625536
  34. Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast.
    Plant Cell. 2004 Mar;16(3):643-57 PMID: 15004270
  35. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo.
    Development. 1999 Apr;126(7):1387-95 PMID: 10068632
  36. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation.
    Genes Dev. 2002 Oct 1;16(19):2566-75 PMID: 12368267
  37. The ubiquitin 26S proteasome proteolytic pathway.
    Annu Rev Plant Biol. 2004;55:555-90 PMID: 15377232
  38. EMBOSS: the European Molecular Biology Open Software Suite.
    Trends Genet. 2000 Jun;16(6):276-7 PMID: 10827456
  39. A gateway cloning vector set for high-throughput functional analysis of genes in planta.
    Plant Physiol. 2003 Oct;133(2):462-9 PMID: 14555774
  40. Embryogenesis: A New Start in Life.
    Plant Cell. 1997 Jul;9(7):989-1000 PMID: 12237371
  41. Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms.
    J Biol Chem. 2004 Feb 20;279(8):6401-13 PMID: 14623884
  42. The origins of genomic duplications in Arabidopsis.
    Science. 2000 Dec 15;290(5499):2114-7 PMID: 11118139
  43. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein.
    Plant J. 1999 Nov;20(4):503-8 PMID: 10607302
  44. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis.
    Gene. 1995 Dec 29;167(1-2):GC1-10 PMID: 8566757
  45. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome.
    Science. 2002 Oct 18;298(5593):611-5 PMID: 12183636
  46. The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development.
    Development. 2000 Jan;127(1):23-32 PMID: 10654597
  47. Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein.
    Mol Biol Cell. 1996 Dec;7(12):2029-44 PMID: 8970163
  48. Differential stability of Arabidopsis D-type cyclins: CYCD3;1 is a highly unstable protein degraded by a proteasome-dependent mechanism.
    Plant J. 2004 May;38(4):616-25 PMID: 15125768
  49. Identification of ubiquitin-like protein-binding subunits of the 26S proteasome.
    Biochem Biophys Res Commun. 2002 Aug 30;296(4):813-9 PMID: 12200120
  50. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning.
    Genes Dev. 2002 Jul 1;16(13):1610-5 PMID: 12101120
  51. Comparative analysis of non-random DNA repair following Ac transposon excision in maize and Arabidopsis.
    Plant J. 1997 Dec;12(6):1419-27 PMID: 9450346
  52. Intrachromosomal excision of a hybrid Ds element induces large genomic deletions in Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2969-74 PMID: 14981243
  53. Inhibition of proteasome activity strongly affects kiwifruit pollen germination. Involvement of the ubiquitin/proteasome pathway as a major regulator.
    Plant Physiol. 2001 Jul;126(3):1150-61 PMID: 11457965
  54. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis.
    Genes Dev. 2001 Apr 1;15(7):902-11 PMID: 11297513
  55. Cell Differentiation and Morphogenesis Are Uncoupled in Arabidopsis raspberry Embryos.
    Plant Cell. 1994 Dec;6(12):1713-1729 PMID: 12244232
  56. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product.
    Cell. 1996 Jan 12;84(1):61-71 PMID: 8548827
  57. The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems.
    Development. 2004 May;131(9):2101-11 PMID: 15073153
  58. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis.
    Science. 1998 Apr 17;280(5362):446-50 PMID: 9545225
  59. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  60. The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling.
    Plant Cell. 2003 Apr;15(4):965-80 PMID: 12671091
  61. Extensive duplication and reshuffling in the Arabidopsis genome.
    Plant Cell. 2000 Jul;12(7):1093-101 PMID: 10899976
  62. Analysis of polyubiquitin conjugates reveals that the Rpn10 substrate receptor contributes to the turnover of multiple proteasome targets.
    Mol Cell Proteomics. 2005 Jun;4(6):741-51 PMID: 15699485
  63. The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo.
    Development. 1998 Feb;125(3):521-31 PMID: 9425146
  64. Multiple associated proteins regulate proteasome structure and function.
    Mol Cell. 2002 Sep;10(3):495-507 PMID: 12408819
  65. Mts4, a non-ATPase subunit of the 26 S protease in fission yeast is essential for mitosis and interacts directly with the ATPase subunit Mts2.
    J Biol Chem. 1997 Oct 10;272(41):25768-77 PMID: 9325304
  66. Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis.
    Mol Biol Cell. 2002 Jun;13(6):1916-28 PMID: 12058059
  67. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements.
    Genes Dev. 1995 Jul 15;9(14):1797-810 PMID: 7622040
  68. Diversity of TITAN functions in Arabidopsis seed development.
    Plant Physiol. 2002 Jan;128(1):38-51 PMID: 11788751
  69. Multiubiquitin chain binding subunit MCB1 (RPN10) of the 26S proteasome is essential for developmental progression in Physcomitrella patens.
    Plant Cell. 1999 Aug;11(8):1457-72 PMID: 10449580
  70. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  71. Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants.
    EMBO J. 1994 Feb 1;13(3):616-24 PMID: 8313906
  72. Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12.
    Plant Cell. 2002 Jan;14(1):17-32 PMID: 11826296
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2005-10-00
Epub
2005-00-16
Pages
2723-37
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1242268
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: product@genelibs.com