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The diverse roles of ubiquitin and the 26S proteasome in the life of plants

Nature Reviews Genetics volume 4, pages 948–958 (2003)Cite this article

Key Points

  • The tagging of proteins with ubiquitin and their subsequent degradation by the 26S proteasome provides a highly regulated proteolysis system that is necessary in all eukaryotes.

  • The ubiquitylation of a target protein involves the sequential action of E1, E2 and E3 enzymes; E3 ubiquitin ligase provides target specificity.

  • Plants use ubiquitin and the 26S proteasome to control a wide variety of developmental processes through the degradation of key cellular regulators.

  • Approximately 5% of the Arabidopsis thaliana genome encodes components of the ubiquitin/26S proteasome system.

  • We discuss the roles of ubiquitin in the regulation of floral development, responses to plant hormones and to pathogens, and in the regulation of photomorphogenesis.

  • The COP9 signalosome (CSN) is intimately connected to the ubiquitin/26S proteasome system and might regulate the activity of SCF-type (and possibly other) E3 ligases.

  • Recent advances, particularly in the fields of hormone signalling and responses to pathogens, have shown just how frequently plants use ubiquitin to regulate cellular processes and indicate that ubiquitin and the 26S proteasome act as regulators in many more, as yet unidentified, plant developmental processes.

Abstract

A tightly regulated and highly specific system for the degradation of individual proteins is essential for the survival of all organisms. In eukaryotes, this is achieved by the tagging of proteins with ubiquitin and their subsequent recognition and degradation by the 26S proteasome. In plants, genetic analysis has identified many genes that regulate developmental pathways. Subsequent analysis of these genes has implicated ubiquitin and the 26S proteasome in the control of diverse developmental processes, and indicates that proteolysis is a crucial regulatory step throughout the life cycle of plants.

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Figure 1: The ABC model of floral organ development and the role of SCFUFO in regulating the B-type gene AP3.
Figure 2: A model for R protein-dependent disease-resistance signalling and the role of SCF and the COP9 signalosome.
Figure 3: The effect of light on Arabidopsis seedling development and the ubiquitylation and protein degradation conferred by the COP/DET/FUS group of proteins.

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Acknowledgements

J.A.S. is supported by a Human Frontiers Science Program long-term fellowship. Research in K.S.'s laboratory is supported in part by grants from the Gatsby Charitable Foundation and the Biotechnology and Biological Sciences Research Council. Related research in X.W.D.'s laboratory is supported by grants from the National Institutes of Health and the National Science Foundation.

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Authors and Affiliations

  1. Deptartment of Molecular, Cellular and Developmental Biology, Yale University, PO Box 208104, 165 Prospect Street, New Haven, 06520-8104, Connecticut, USA

    James A. Sullivan & Xing Wang Deng

  2. The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

    Ken Shirasu

Authors
  1. James A. Sullivan
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Correspondence to Xing Wang Deng.

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DATABASES

TAIR

APETALA3

Axr1

CIO1

COP

COP10

DET

FUS

LEAFY

NIM1

PISTILLATA

RAR1

RGA

SGT1α

SGT1b

SKP1

SLEEPY1

ubiquitin

UNUSUAL FLORAL ORGANS

UPL3

UK CropNet

Mla6

Mla12

FURTHER INFORMATION

Xing Wang Deng's laboratory

Glossary

PROTO-ONCOGENE

A gene that has the potential to change into an active cancer-causing oncogene.

ENDOCYTOSIS

The uptake of extracellular materials within membrane-bound vesicles by cells.

ISOPEPTIDE BOND

The covalent linkage that joins amino-acid residues through an amide bond.

THIOESTER LINKAGE

A non-covalent chemical bond between two proteins formed through thiolester.

CONJUGATION

The addition of ubiquitin moieties to a growing polyubiquitin chain.

SENESCENCE

Regulated death of an organ or a cell after its normal physiological function.

CHELATION

The process by which an organic chemical bonds with metal ions and thereby removes them from solutions.

WHORLS

A specific layer of flower organs that is generated through floral meristem activity.

SEPALS

The protective outer layer of flower.

STAMENS

The third layer of flower that bears the male gametophyte that produces pollen.

CARPELS

The fourth whorl of flower that bears the female gametophyte.

TRANSFORMATION

The change from one developmental pattern to another.

APICAL DOMINANCE

Concentration of growth at the tip of a plant shoot, where a terminal bud exerts partial inhibition of auxiliary bud growth.

ALEURONE CELLS

A cell type in cereal kernals that undergoes highly regulated cell death to release stores of minerals and nutrients to the developing embryo.

PHENOCOPY

The production of a phenotype, which closely resembles a phenotype that normally results from specific gene expression or from gene mutation.

POWDERY MILDEW

A group of plant diseases that are caused by the growth of fungal mycelium and the production of spores on the surface of plant tissues.

DENEDDYLATION

The removal of the ubiquitin-like modifier NEDD8 (also called RUB) from a protein.

HISTONE DEACETYLASE

The enzyme that removes acetyl groups from lysine residues in the DNA-binding histone group of proteins.

SKOTOMORPHOGENIC

Developmental pattern followed by seedlings in the absence of light.

HYPOCOTYLS

The stem of a seedling.

COTYLEDONS

The leaves of a seedling formed during embryonic development.

PHOTOMORPHOGENIC

Developmental pattern followed by seedlings in the presence of light.

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Sullivan, J., Shirasu, K. & Deng, X. The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4, 948–958 (2003). https://doi.org/10.1038/nrg1228

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