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The ubiquitin–26S proteasome system at the nexus of plant biology

Nature Reviews Molecular Cell Biology volume 10, pages 385–397 (2009)Cite this article

Key Points

  • The ubiquitin-26S proteasome system (UPS) is one of the most complex and pervasive pathways of intracellular protein regulation in plants.

  • Genomic estimates indicate that as much as 6% of the Arabidopsis thaliana transcriptome is devoted to expressing UPS components, with most of these genes encoding ubiquitin ligases (>1,400 loci).

  • Genetic analyses have recently connected the UPS to much of plant hormone signalling, regulation of chromatin structure and transcription, tailoring morphogenesis, responses to environmental challenges, self recognition and the war between pathogens and their plant hosts.

  • In several signalling pathways, components involved in ubiquitin ligation have been shown to act as receptors for hormones and light.

  • Recent proteomic studies have identified a catalogue of plant proteins that are modified by ubiquitylation in planta and have identified various types of polyubiquitin chains.

  • Why the UPS system is so large in plants is currently unclear. Possibilities include their sessile growth habit, which might require additional levels of regulation, the ancient genome duplications common during plant evolution, roles of the UPS in innate immunity and, for annual plants, their reliance on the UPS to confine their life cycle to short growing seasons.

Abstract

Plants, like other eukaryotes, rely on proteolysis to control the abundance of key regulatory proteins and enzymes. Strikingly, genome-wide studies have revealed that the ubiquitin-26S proteasome system (UPS) in particular is an exceedingly large and complex route for protein removal, occupying nearly 6% of the Arabidopsis thaliana proteome. But why is the UPS so pervasive in plants? Data accumulated over the past few years now show that it targets numerous intracellular regulators that have central roles in hormone signalling, the regulation of chromatin structure and transcription, tailoring morphogenesis, responses to environmental challenges, self recognition and battling pathogens.

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Figure 1: Phylogenetic comparison of the BTB protein superfamily in plants.
Figure 2: Roles of specific E3s in hormone signalling and photoperiod measurement.
Figure 3: Control of ethylene synthesis and perception by the UPS.
Figure 4: Control of Agrobacterium infection by VirF.
Figure 5: Control of self-incompatibility in flowers by the ubiquitin-26S proteasome system.

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Acknowledgements

The author thanks various members of the laboratory for helpful discussions and apologizes to those whose work was not cited because of space constraints. Research in the Vierstra laboratory is supported by grants from the US Department of Energy Basic Energy Sciences Program, the US Department of Agriculture Cooperative State Research, Education and Extension Service, the US National Science Foundation Arabidopsis 2010 Program, and the University of Wisconsin College of Agriculture and Life Sciences.

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  1. Department of Genetics, 425G Henry Mall, University of Wisconsin-Madison, Madison, 53706, Wisconsin, USA

    Richard D. Vierstra

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Glossary

Ubiquitin fold

The three-dimensional protein structure that is characteristic of ubiquitin and related proteins. Its core domain consists of a five-stranded β-sheet that diagonally cradles an α-helix.

Abscisic acid

A plant hormone derived from carotenoids that helps plants respond to stress and prevents precocious germination of seeds.

RING domain

A cross-braced structure formed by an octet of Cys residues and His residues that chelate two zinc atoms. Its threedimensional structure creates a pocket that binds the ubiquitin-E2 intermediate during the ubiquitylation of substrates.

COP9-signalosome

A multi-subunit protein complex that is structurally related to the lid of the 26S proteasome. One subunit removes the ubiquitin fold protein RUB1 from the cullin subunit in CRL E3s.

Auxin

A plant hormone related to indole3-acetic acid (IAA) that regulates plant cell elongation, the activity of the shoot and root meristems and vascular development.

Jasmonic acid

A plant hormone related to oxylipins that is important for plant development and protection from biotic challenges.

Gibberellin

A steroid hormone that promotes cell division and seed germination in plants.

Ethylene

A gaseous plant hormone that inhibits plant growth in response to stress and stimulates fruit ripening.

Trichome

A pointed hair cell (often with three branches) that extends from the surface of aerial portions of plants to provide protection from herbivores and the environment.

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Vierstra, R. The ubiquitin–26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10, 385–397 (2009). https://doi.org/10.1038/nrm2688

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