Ubiquitin-Mediated Control of Plant Hormone Signaling

Abstract

The ubiquitin-proteasome system (UPS) plays a role in nearly every aspect of plant biology. The wealth of emerging data demonstrates that regulated protein degradation rivals the well-studied area of transcriptional regulation for importance in cellular regulation. In this Update, we will highlight current research findings that illustrate the contributions of the UPS to phytohormone signaling. We will also consider outstanding questions and discuss possible experimental approaches that will increase our understanding of regulated protein degradation. UPS activity involves a three-step enzymatic cascade between E1, E2, and E3 enzymes that results in the covalent transfer of ubiquitin to target proteins. This process can result in different outcomes, including (1) proteolytic degradation by the 26S proteasome or reversible, nonproteolytic regulatory events. Current plant genome annotations indicate that most species can produce over 1,000 different UPS components; E3 ligase family proteins are the most abundant (Du et al., 2009; Vierstra, 2009). Thus, the potential scope of the UPS is extensive. E3 ligases provide specificity by directly controlling the transfer of ubiquitin to the target substrate and have been classified into four groups based on their complex composition and modes of action: HECT, RING, U-box, and cullin-RING ligases (CRLs; Vierstra, 2009). CRLs are multisubunit ligases that can be further subdivided into four groups based on a variable target recognition module: (1) F-box proteins in the case of S-phase kinase-associated protein1-cullin1-F-box (SCF) ligases; (2) bric-a-brac-tramtrak-broad complex (BTB) proteins that define the BTB group of E3s; (3) the DNA damage-binding (DDB) class that utilizes WD40 domain-containing DWD proteins; and (4) the anaphase-promoting complex category that contains several interchangeable recognition proteins (Vierstra, 2009). Altogether, these enzymatic modules are incredibly diverse, and many of their targets are currently unknown. The phytohormones are small molecule regulators that collectively impact every aspect of plant growth and development. They regulate genetically determined aspects of development such as organ development as well as pathogen response, integration of environmental cues such as light and temperature, and regulation of circadian clock output (Ho et al., 2008; Vierstra, 2009; Lee and Lee, 2012). Recent discoveries highlight the particular importance of UPS action in phytohormone signaling. In fact, UPS-mediated protein degradation has been implicated or demonstrated for every plant hormone, including abscisic acid (ABA), auxin, brassinosteroid (BR), cytokinin, ethylene, GA, jasmonic acid (JA), and strigolactone (SL). Notably, the UPS is also very important for steroid hormone signaling in humans (Lee and Lee, 2012). While some plant hormones undergo long-distance transport and thus have different sites of synthesis and action (e.g. auxin, SL), others appear to be synthesized and function in the same tissue (e.g. BR). As we will discuss in more detail below, one of the major functions of UPS pathways in hormone signaling is the selective destruction of proteins whose concentrations must vary with time and alterations in the state of the cell. UPS action appears to regulate hormone biosynthesis, transport, and perception and thus provides a direct mechanism to control the magnitude and duration of hormone signaling (Figs. 1 and 2). Detailed studies of UPS function in phytohormone pathways have revealed a number of patterns. First, most of the hormone-related UPS targets described to date are proteins associated with transcription. Furthermore, many of the known target transcription factors are classified as repressors and contain ETHYLENE RESPONSE FACTOR-associated amphiphilic repression domains. This includes the auxin/indole-3-acetic acid (Aux/IAA; auxin), jasmonate-ZIM domain (JAZ; JA), and BRASSINAZOLE RESISTANT1 (BZR1; BR) proteins (Kagale et al., 2010). Second, a number of hormones directly control ligase-substrate interactions (e.g. auxin, JA, and GA). The protein degradation mechanisms involved in auxin, JA, and GA signaling are strikingly similar (Fig. 1, A, D, and E). Additionally, in the case of both auxin and JA, the F-box proteins responsible for target proteolysis are themselves part of the hormone receptor complex. UPS components controlling BR and ethylene signaling also appear to be superficially similar. We will describe the types of E3 ligases and their target proteins (when known) that are active in Arabidopsis (Arabidopsis thaliana) in more detail below. The hormones are organized with the aim of highlighting the mechanistic similarities and differences of UPS action. Conservation of these pathways in other plant species is discussed separately at the end of the article. Conserved and diverse UPS degradation mechanisms control hormone signaling (ABA is considered separately due to the abundance of UPS components; s