Gibberellin Signaling: Biosynthesis, Catabolism, and Response Pathways

Abstract

The power of molecular genetics has dramatically advanced our understanding of all aspects of gibberellin (GA) signaling. Many genes encoding GA response pathway components have been identified using Arabidopsis and cereal mutants, and more elaborate genetic screens are producing additional mutants that are providing new insights into this pathway. Now, a confluence of new approaches, such as functional genomics and proteomics, promises even more rapid progress in unraveling the physiology and biochemistry of GA-regulated processes. New levels of regulation are being identified that indicate that the GA response pathway is linked tightly to its biosynthesis and catabolism. Furthermore, the GA metabolism and response pathways integrate with other signaling pathways to regulate plant growth and development, and the interaction between these response pathways is likely to be extremely complex. Several recent reviews have described GA biosynthesis and catabolism (Lange, 1998; Kamiya and García-Martínez, 1999; Hedden and Phillips, 2000; Yamaguchi and Kamiya, 2000) and the GA response pathway (Thornton et al., 1999b; Lovegrove and Hooley, 2000; Sun, 2000; Richards et al., 2001). This review focuses on recent results in the field of GA signaling. We begin by considering the aspects of the homeostatic and developmental control of GA biosynthesis and catabolism that relate to signaling. Then, we discuss components of the GA response pathway that have been identified primarily through the analysis of mutants exhibiting altered GA responses. We conclude with a summary of the cereal aleurone, which has proven to be an excellent model system for studies of GA signaling. GAs form a large family of diterpenoid compounds, some of which are bioactive growth regulators, that control such diverse developmental processes as seed germination, stem elongation, leaf expansion, trichome development, and flower and fruit development (Davies, 1995). There is much evidence that environmental stimuli, including light and temperature, can affect plant processes by either changing the GA concentrations and/or altering the responsiveness to GA (reviewed by Davies, 1995; Kamiya and García-Martínez, 1999). Major GA Biosynthetic and Catabolic Pathways in Higher Plants. The enzyme names are shown in boldface below or to the right of each arrow. GA9 and GA20 also can be converted to GA51 and GA29 by GA2ox. GA4 and GA1 are the bioactive GAs, and GA34 and GA8 are their inactive catabolites. The biosynthesis of GA in higher plants can be divided into three stages: (1) biosynthesis of ent-kaurene in proplastids; (2) conversion of ent-kaurene to GA12 via microsomal cytochrome P450 monooxygenases; and (3) formation of C20- and C19-GAs in the cytoplasm (Figure 1). In the first stage, geranylgeranyl diphosphate, which serves as a common precursor for diterpenes (e.g., GAs and the phytol chain of chlorophyll) and tetraterpenes (carotenoids), is synthesized by either a mevalonate-dependent or a nonmevalonate pathway (reviewed by Lange, 1998; Hedden and Phillips, 2000). Geranylgeranyl diphosphate then is converted to ent-kaurene in a and by diphosphate and ent-kaurene with diphosphate as the In the of the by by ent-kaurene and which can be converted to by In the of GA GA12 and are converted to GA and bioactive GAs, including GA1 and by a of by GA and GA 1). GAs have been identified in higher and a are (e.g., and and Phillips, 2000). Many of the other GAs are or of bioactive the pathways in plants that to the formation of GA1 and The of bioactive GAs can be by the of their and the conversion to inactive by which is by GA 1). The of the first in the GA is by and In extremely of are plant development, and the of this is et al., including and higher of The of is to that of the of is much higher that of et al., Yamaguchi and Sun, that the of ent-kaurene is primarily by the and of The of of the and the of the that as a the and of the of GA and each is by a in plant and their is regulation by the of the GA response pathway (reviewed by Hedden and Phillips, 2000). genes are in and are in all et al., In the and each is by a and each also (reviewed by Hedden and Phillips, 2000). of these genes in plants in some the concentrations of bioactive that the regulation of these genes is in in the of the pathway (reviewed by Hedden and Phillips, 2000; Yamaguchi and Kamiya, 2000). of regulation of the GA pathway in the of the pathway (Figure 1). studies that ent-kaurene is synthesized in the and are in this and Kamiya, et al., is a cytochrome P450 enzyme that is to with the (reviewed by and is the ent-kaurene is to the studies of and in that and are to the and are with the et al., In using that is into the the P450 enzyme is on the of the new a for to its these studies the of to the in and some also in the cytoplasm in the of et al., these to in the plants the likely of the the to be is on the in of the of GA in GA response mutants indicate that the of responsiveness