Ubiquitin ligases mediate growth and development by promoting protein death

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The ubiquitin proteasome system (UPS) allows plants to effectively and efficiently alter their proteome so as to ensure developmental plasticity and environmental adaptation. Recent work has demonstrated that the UPS is an integral part of multiple hormone-signaling pathways, which modulate cell growth and differentiation. In response to variation in hormone levels, the UPS regulates the abundance of signaling factors, mainly hormone-responsive transcription factors, which mediate cellular responses. Recent exciting studies have shown that hormones directly or indirectly modulate substrate ubiquitination by regulating E3-substrate interaction. Other avenues of regulation include regulating E3 mRNA abundance.

Introduction

A plant's ability to alter growth and development relies heavily on proteomic plasticity. Regulated ubiquitin-mediated and proteasome-mediated degradation, therefore, plays a crucial role in enabling plants to alter their proteome in order to differentiate into the appropriate cell, tissue and/or organ type and to maximize their chances of survival in different environments. To accomplish this, hormones act as important integrators of endogenous and exogenous signals.

Genetic approaches to elucidate the molecular mechanisms of hormone action have revealed direct links between hormone production, perception, signal transduction and outputs and the ubiquitin proteasome system (UPS). Ubiquitin-mediated degradation of proteins in the perception of, and/or response to, hormonal stimuli is at the core of many hormone-signaling pathways. With several recent exciting advances in understanding UPS-mediated regulation of hormone signaling, this review will focus mainly on new discoveries in the past few years on E3 ligases implicated in hormonal responses. E3 components implicated in developmental processes but not linked to a specific hormonal pathway are listed in Table 1, while those linked to a specific pathway are listed in Table 2. The reader is referred to several recent reviews for discussion of the role of the UPS in photomorphogenesis [1] and biotic stress [2, 3].

Section snippets

Ubiquitin E3 ligases

The UPS pathway includes the E1 (ubiquitin activating), E2 (ubiquitin conjugating) and E3 (ubiquitin ligase) enzymes required for covalent attachment of the 76-aa protein ubiquitin to a substrate protein, as well as the proteins involved in recognition, transport and catabolism of the ubiquitinated substrate (Figure 1). For several reasons, ubiquitin is a versatile post-translational modification. First, a single ubiquitin has multiple protein-interaction surfaces. Second, one, a few or many

Auxin

Utilization of the UPS to control hormone responsiveness is epitomized by the auxin-signaling pathway. Auxin, of which the major endogenous form is indole-3-acetic acid (IAA), plays a crucial role in regulating cell growth, division and differentiation, root elongation, apical dominance and other developmental processes. Auxin alters the RNA profile, presumably to effect developmental changes and the UPS is involved in regulating these transcriptional changes. At the centre of the auxin

Multiple E3s probably regulate hormone signal transduction pathways

The cellular response to a single hormone usually involves the function of multiple ubiquitin E3 ligases, and in some cases different classes of E3s are used to regulate the same signaling pathway (Table 2). For example, the role of the UPS in auxin signaling is not limited to the SCFTIR1/ABF1-5 E3s. The RING E3, SINAT5, ubiquitinates NAC1, a transcriptional activator that functions downstream of TIR1 to promote auxin-mediated lateral root development [49]. Regulated proteolysis is also

The UPS regulates hormone synthesis

In addition to modulating hormonal signaling component abundance, the UPS can modulate hormone synthesis to alter development. ACC synthase activity is the primary control point in ethylene synthesis. Type 2 ACC synthases, such as ACS5, interact with Ethylene Overproducer (ETO) 1, requiring ACS5 C-terminal residues [51, 52•]. ETO1 contains a BTB domain found in substrate specificity subunits of CUL3-based CRLs and has been shown to associate with CUL3 [53]. ABA synthesis is affected in plants

Conclusions

The link between hormone synthesis, perception, response and UPS has been firmly established. As more E3s are functionally characterized, additional E3 ligases that play pivotal roles in hormone signaling will undoubtedly be identified. The significance of ubiquitin ligases to plant development is in no way limited to hormone pathways, the focus of this review. In addition, the large number and diversity of plant ubiquitin ligases suggest that E3 enzymes control the abundance, as well as

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Note added in proof

Chini et al also identified the JAZ proteins (Nature 448: 661–671). Zhang et al report on a RING E3 ligase in ABA response (Plant Cell 19: 1912–1929).

Acknowledgements

The authors apologize to those whose work could not be included because of space constraints. The authors would like to thank Sara Hotton for comments. Research in Callis laboratory is supported by the National Science Foundation (2010 Program MCB-0519970) and the Department of Energy (DE-FG02-03ER15416). Research in the Stone laboratory is supported by the Natural Sciences and Engineering Research Council of Canada and the Human Frontier Science Program.

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