Mechanisms of Cross Talk between Gibberellin and Other Hormones

Abstract

It has always been clear that different plant hormones affect overlapping processes, such that the output of plant hormone action depends on specific hormone combinations rather than on the independent activities of each. In the last two decades, numerous components of the signal transduction pathways of various plant hormones have been identified, leading to the elucidation of partial or entire signaling cascades. These findings have provided the tools to begin addressing the mechanisms underlying the cross talk among different hormone signal transduction pathways. Such cross talk involves diverse mechanisms, which act at both the hormone response and biosynthesis levels, creating a delicate response network. In this review, we describe how gibberellin (GA) interacts with other plant hormones, concentrating on its interactions with abscisic acid (ABA), auxin, ethylene, and cytokinin. Although evidence for interactions of GA with brassinosteroids (Bouquin et al., 2001) and jasmonate (Traw and Bergelson, 2003) also exists, we focus on studies addressing the mechanisms governing the cross talk. GAs regulate various developmental processes throughout the life cycle of the plant, from seed germination through leaf expansion, stem elongation, flower induction, and development to seed development (Sun and Gubler, 2004). As the interactions between GA and other hormones involve components from the GA biosynthetic and response pathways, we first briefly introduce a few relevant players in these pathways. For a more comprehensive description of these pathways, see recent reviews (Hedden and Phillips, 2000; Sun and Gubler, 2004; Hartweck and Olszewski, 2006; Lange and Lange, 2006; Razem et al., 2006). The GA biosynthetic pathway has been elucidated by a combination of biochemical and genetic approaches. The first few steps of the pathway, from trans-geranylgeranyl diphosphate to GA12-aldehyde, are common to all species. The final steps to produce active GAs are species specific but in most cases require activity of the GA 20-oxidase (GA20ox) and GA3ox enzymes. In contrast, the enzyme GA2ox antagonizes GA activity by deactivating GAs. The level of endogenous active GA is governed by feedback regulation, where active GAs suppress the expression of the GA20ox and GA3ox genes and promote the expression of the GA2ox gene. Studies of GA signal transduction, using genetic approaches, have led to the identification of positive and negative signaling components (Sun and Gubler, 2004). The most extensively characterized among these are the DELLA proteins, a class of nuclear proteins that belong to the GRAS family of transcriptional regulators and act as suppressors of GA signaling. The molecular mechanism by which DELLA proteins suppress GA responses is not yet clear. The Arabidopsis (Arabidopsis thaliana) genome contains five DELLA genes (REPRESSOR OF ga1-3 [RGA], GA INSENSITIVE [GAI], RGA LIKE1 [RGL1], RGL2, and RGL3), whereas in the rice (Oryza sativa) genome, only one family member has been identified (SLENDER1 [SLR1]; Itoh et al., 2002). A major breakthrough in our understanding of the GA-signaling cascade has been the recent discovery of the soluble GA receptor GA INSENSITIVE DWARF1 (GID1) in rice and Arabidopsis (Ueguchi-Tanaka et al., 2005; Nakajima et al., 2006; Griffiths et al., 2007). GA binding to GID1 triggers its interaction with the DELLA domain of the DELLA proteins (Griffiths et al., 2007). This interaction stimulates binding of the DELLA proteins to an SCF E3 ubiquitin ligase via specific F-box proteins (GID2/SLY), leading to polyubiquitination and degradation of the DELLA protein by the 26S proteosome (Sasaki et al., 2003; Dill et al., 2004; Griffiths et al., 2007). While this relatively simple GA-signaling cascade involves three major players, a receptor, a DELLA protein, and an F-box protein, other studies have identified additional factors that affect GA responses (Hartweck and Olszewski, 2006). One of these is the GA response inhibitor SPINDLY (SPY; Jacobsen and Olszewski, 1993; Filardo and Swain, 2003). The SPY protein resembles mammalian enzymes that modify proteins posttranslationally by a specific type of glycosylation, termed tetratricopeptide repeat-containing Ser and Thr-O-linked GlcNAc transferases (OGT). OGT transfers the single sugar moiety GlcNAc from UDP-GlcNAc to specific Ser/Thr residues via an O-linkage. This posttranslational modification can affect protein localization, phosphorylation, interaction with other proteins, and/or stability (Wells et al., 2001). While there is no direct biochemical evidence for the interaction of SPY with the DELLA proteins, genetic evidence suggests that SPY is required for DELLA's GA response suppression activity (Hartweck and Olszewski, 2006; Silverstone et al., 2007). GA interacts positively and negatively with other plant hormones throughout the plant's life cycle. Some of the effects are shown. CK, Cytokinin. Network of interactions between GA and ABA.