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PMID: 11826296 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12.

The Plant cell ·Vol. 14 ·No. 1 ·2002-01-00 ·Pages 17-32

Smalle J, Kurepa J, Yang P, Babiychuk E, Kushnir S, Durski A, Vierstra RD

Abstract

The 26S proteasome is an ATP-dependent eukaryotic protease responsible for degrading many important cell regulators, especially those conjugated with multiple ubiquitins. Bound on both ends of the 20S core protease is a multisubunit regulatory particle that plays a crucial role in substrate selection by an as yet unknown mechanism(s). Here, we show that the RPN12 subunit of the Arabidopsis regulatory particle is involved in cytokinin responses. A T-DNA insertion mutant that affects RPN12a has a decreased rate of leaf formation, reduced root elongation, delayed skotomorphogenesis, and altered growth responses to exogenous cytokinins, suggesting that the mutant has decreased sensitivity to the hormone. The cytokinin-inducible genes CYCD3 and NIA1 are upregulated constitutively in rpn12a-1, indicating that feedback-inhibitory mechanisms also may be altered. rpn12a-1 seedlings also showed changes in auxin-induced growth responses, further illustrating the close interaction between auxin and cytokinin regulation. In yeast, RPN12 is necessary for the G1/S and G2/M transitions of the cell cycle, phases that have been shown to be under cytokinin control in plants. We propose that RPN12a is part of the Arabidopsis 26S proteasome that controls the stability of one or more of the factors involved in cytokinin regulation.

MeSH Terms
Adenine/analogs & derivatives,pharmacology Amino Acid Sequence Arabidopsis/drug effects,genetics,growth & development Arabidopsis Proteins/genetics,metabolism Cyclin D3 Cyclins/genetics,physiology Cytokinins/pharmacology DNA, Bacterial/genetics Gene Expression Regulation, Plant/drug effects Genetic Complementation Test Indoleacetic Acids/pharmacology Kinetin Mitosis/genetics,physiology Molecular Sequence Data Mutagenesis, Insertional Mutation Peptide Hydrolases/genetics,metabolism Plant Growth Regulators/pharmacology Plant Structures/drug effects,genetics,growth & development Proteasome Endopeptidase Complex Protein Subunits Sequence Homology, Amino Acid Ubiquitins/metabolism
Chemicals
Arabidopsis Proteins Cyclin D3 Cyclins Cytokinins DNA, Bacterial Indoleacetic Acids Plant Growth Regulators Protein Subunits RPN12 protein, Arabidopsis T-DNA Ubiquitins Peptide Hydrolases Proteasome Endopeptidase Complex ATP dependent 26S protease Adenine Kinetin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Smalle Jan
Cellular and Molecular Biology Program, Department of Horticulture, University of Wisconsin-Madison, 1575 Linden Drive, Madison, WI 53706, USA.
Kurepa Jasmina
Yang Peizhen
Babiychuk Elena
Kushnir Sergei
Durski Adam
Vierstra Richard D
References (55)
55 references, click to expand
  1. Cytokinin activation of Arabidopsis cell division through a D-type cyclin.
    Science. 1999 Mar 5;283(5407):1541-4 PMID: 10066178
  2. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  3. Sequences within both the N- and C-terminal domains of phytochrome A are required for PFR ubiquitination and degradation.
    Plant J. 1999 Jan;17(2):155-67 PMID: 10074713
  4. Cyclin-dependent kinases and cell division in plants- the nexus
    Plant Cell. 1999 Apr;11(4):509-22 PMID: 10213774
  5. Structure and functional analysis of the 26S proteasome subunits from plants.
    Mol Biol Rep. 1999 Apr;26(1-2):137-46 PMID: 10363660
  6. Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome.
    Plant J. 1999 Jun;18(5):529-39 PMID: 10417703
  7. 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
  8. 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
  9. Physical association of ubiquitin ligases and the 26S proteasome.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2497-502 PMID: 10688918
  10. Function of the ubiquitin-proteasome pathway in auxin response.
    Trends Biochem Sci. 2000 Mar;25(3):133-8 PMID: 10694884
  11. Induction of competence for elicitation of defense responses in cucumber hypocotyls requires proteasome activity.
    Plant J. 2000 Feb;21(3):311-6 PMID: 10758482
  12. The Arabidopsis Cdc2a-interacting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclin-dependent kinase activity in vitro.
    Plant J. 2000 Feb;21(4):379-85 PMID: 10758489
  13. Triggering the cell cycle in plants.
    Trends Cell Biol. 2000 Jun;10(6):245-50 PMID: 10802540
  14. The 26S proteasome: a molecular machine designed for controlled proteolysis.
    Annu Rev Biochem. 1999;68:1015-68 PMID: 10872471
  15. Proteasomal turnover of p21Cip1 does not require p21Cip1 ubiquitination.
    Mol Cell. 2000 Feb;5(2):403-10 PMID: 10882081
  16. Protein degradation in signaling.
    Curr Opin Plant Biol. 2000 Oct;3(5):381-6 PMID: 11019805
  17. The Arabidopsis D-type cyclins CycD2 and CycD3 both interact in vivo with the PSTAIRE cyclin-dependent kinase Cdc2a but are differentially controlled.
    J Biol Chem. 2001 Mar 9;276(10):7041-7 PMID: 11096103
  18. The cellular level of PR500, a protein complex related to the 19S regulatory particle of the proteasome, is regulated in response to stresses in plants.
    Mol Biol Cell. 2001 Feb;12(2):383-92 PMID: 11179422
  19. Identification of CRE1 as a cytokinin receptor from Arabidopsis.
    Nature. 2001 Feb 22;409(6823):1060-3 PMID: 11234017
  20. 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
  21. EID1, an F-box protein involved in phytochrome A-specific light signaling.
    Genes Dev. 2001 Apr 15;15(8):939-44 PMID: 11316788
  22. Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response.
    Science. 2001 May 18;292(5520):1379-82 PMID: 11337587
  23. Auxin-cytokinin interactions in higher plants: old problems and new tools.
    Trends Plant Sci. 1997 Sep;2(9):351-6 PMID: 11540614
  24. The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana.
    Plant J. 2001 Sep;27(5):393-405 PMID: 11576424
  25. 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
  26. A Role for Cytokinins in De-Etiolation in Arabidopsis (det Mutants Have an Altered Response to Cytokinins).
    Plant Physiol. 1994 Feb;104(2):339-347 PMID: 12232085
  27. Regulation of Flavonoid Biosynthetic Genes in Germinating Arabidopsis Seedlings.
    Plant Cell. 1992 Oct;4(10):1229-1236 PMID: 12297632
  28. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination.
    Nature. 1992 Dec 10;360(6404):597-9 PMID: 1334232
  29. Cytokinins and auxins control the expression of a gene in Nicotiana plumbaginifolia cells by feedback regulation.
    Plant Cell. 1992 Apr;4(4):451-61 PMID: 1498603
  30. A new essential gene of Saccharomyces cerevisiae, a defect in it may result in instability of nucleus.
    Exp Cell Res. 1992 May;200(1):48-57 PMID: 1563492
  31. Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant.
    EMBO J. 1990 Dec;9(13):4543-9 PMID: 2176155
  32. Sequence organization and developmental expression of an interspersed, repetitive element and associated single-copy DNA sequences in Dictyostelium discoideum.
    Mol Cell Biol. 1985 Aug;5(8):2123-30 PMID: 2427932
  33. Increased endogenous cytokinin in the Arabidopsis amp1 mutant corresponds with de-etiolation responses.
    Planta. 1996 Apr;198(4):549-556 PMID: 28321665
  34. Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae.
    EMBO J. 1995 Jul 3;14(13):3105-15 PMID: 7621825
  35. A novel cytokinin-resistant mutant of Arabidopsis with abbreviated shoot development.
    Planta. 1995;195(3):440-9 PMID: 7766046
  36. Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings.
    Plant Physiol. 1995 Apr;107(4):1075-82 PMID: 7770519
  37. A FUSCA gene of Arabidopsis encodes a novel protein essential for plant development.
    Plant Cell. 1994 Jan;6(1):25-41 PMID: 8130643
  38. Characterization of the function of the NIN1 gene product of Saccharomyces cerevisiae.
    Exp Cell Res. 1994 Apr;211(2):203-11 PMID: 8143766
  39. Homologues of wheat ubiquitin-conjugating enzymes--TaUBC1 and TaUBC4 are encoded by small multigene families in Arabidopsis thaliana.
    Plant Mol Biol. 1994 Feb;24(4):651-61 PMID: 8155884
  40. Arabidopsis MBP1 gene encodes a conserved ubiquitin recognition component of the 26S proteasome.
    Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):856-60 PMID: 8570648
  41. A conditional lethal mutant in the fission yeast 26 S protease subunit mts3+ is defective in metaphase to anaphase transition.
    J Biol Chem. 1996 Mar 8;271(10):5704-11 PMID: 8621436
  42. 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
  43. Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress, and hormonal treatments.
    Plant Cell Physiol. 1997 Apr;38(4):463-70 PMID: 9177032
  44. Efficient gene tagging in Arabidopsis thaliana using a gene trap approach.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12722-7 PMID: 9356517
  45. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26 S proteasome subunit Mcb1.
    J Biol Chem. 1998 Jan 23;273(4):1970-81 PMID: 9442033
  46. 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
  47. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.
    Science. 1998 May 15;280(5366):1091-4 PMID: 9582125
  48. Molecular organization of the 20S proteasome gene family from Arabidopsis thaliana.
    Genetics. 1998 Jun;149(2):677-92 PMID: 9611183
  49. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis.
    Plant Cell. 1998 Jun;10(6):1009-19 PMID: 9634588
  50. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate.
    FEBS Lett. 1998 Jun 16;429(3):259-62 PMID: 9662428
  51. Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle.
    Trends Biochem Sci. 1998 Jul;23(7):244-5 PMID: 9697412
  52. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3.
    Cell. 1998 Sep 4;94(5):615-23 PMID: 9741626
  53. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid.
    Plant J. 1998 Aug;15(4):501-10 PMID: 9753775
  54. The ubiquitin system.
    Annu Rev Biochem. 1998;67:425-79 PMID: 9759494
  55. Cell cycle -dependent proteolysis in plants. Identification Of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor mg132
    Plant Cell. 1998 Dec;10(12):2063-76 PMID: 9836745
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2002-01-00
Pages
17-32
Language
English
Region
England
NLM ID
9208688
PMCID
PMC150548
Subset
IM
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