Gibberellin Signaling: A Theme and Variations on DELLA Repression

Abstract

GAs are a family of tetracyclic diterpenoid plant hormones that stimulate plant growth and developmental transitions. As sessile organisms, plants rely on developmental plasticity to respond to environmental challenges. Plant hormones regulate developmental responses to diverse environmental stimuli such as changes in light, temperature, moisture, animal feeding, and disease pressure. GAs stimulate seed germination in response to changes in light, temperature, and moisture (Koornneef and van der Veen, 1980; Yamauchi et al., 2004; Seo et al., 2009). GA also stimulates stem elongation and leaf expansion through cell expansion and cell division in response to light or dark (photomorphogenesis and skotomorphogenesis; Ogawa et al., 2003; Alabadí et al., 2008; Feng et al., 2008; de Lucas et al., 2008; Gallego-Bartolomé et al., 2011). GA stimulates developmental transitions from meristematic to shoot growth, from juvenile to adult leaf development, and from vegetative growth to flowering, and also stimulates aspects of flower development (Telfer et al., 1997; Yu et al., 2004; Galinha et al., 2009). The appropriate regulation of these events is essential to the survival of plant species and to successful crop production. GA stimulates many aspects of plant growth and development by lifting DELLA (Asp-Glu-Leu-Leu-Ala) protein repression of these events. This article will review multiple biochemical mechanisms for the regulation of and response to DELLA repression. Studies using plants with altered GA biosynthesis or catabolism have resulted in a wealth of knowledge of the diverse roles of GA in plant growth and development (for review, see Sun and Gubler, 2004; Yamaguchi, 2008). GA biosynthesis enzyme mutants of dicots and monocots are GA sensitive, showing defects in growth and development that are rescued by GA application. GA-sensitive mutants of rice (Oryza sativa) and barley (Hordeum vulgare) exhibit dwarfism, infertility, and failure to mobilize stored reserves during seed germination through α-amylase induction (Zwar and Chandler, 1995; Chandler and Robertson, 1999; Sakamoto et al., 2004). Similar phenotypes are seen in Arabidopsis (Arabidopsis thaliana) mutants affecting enzymes acting later in the biosynthesis pathway, GA 3-oxidase (GA3ox) and GA20ox (Hedden and Phillips, 2000; Plackett et al., 2012). Since GA3ox and GA20ox belong to multigene families, single mutants are fertile semidwarves. In Arabidopsis and tomato (Solanum lycopersicum), mutants affecting early GA biosynthesis enzymes such as ent-copalyl diphosphate synthase (Sun and Kamiya, 1994) cause failure in seed germination, growth as a dark green dwarf, failure to transition to flowering under short days, and partial to complete infertility (Koornneef and van der Veen, 1980; Karssen et al., 1989; Wilson et al., 1992). Overexpression of the gene encoding the GA catabolic enzyme GA2ox increases GA turnover, leading to reduced grain germination and α-amylase induction in wheat (Triticum aestivum; Appleford et al., 2007) and to failures in seed development and pollen tube growth in Arabidopsis (Singh et al., 2002). GA signaling is often controlled through direct regulation of hormone accumulation mediated by changes in GA20ox, GA3ox, and GA2ox expression in response to environmental or developmental stimuli. This is logical, as the hormone is the first step in a hormone signaling pathway. Stimulation of Arabidopsis seed germination by red light or cold imbibition and inhibition of germination by far-red light are associated with increased and decreased GA accumulation, respectively (for review, see Seo et al., 2009). Far-red light inhibits seed germination by inducing GA turnover through GA2ox2 and inhibiting the GA biosynthesis GA3ox genes, whereas red light or cold stimulates germination by inducing the biosynthesis genes GA3ox or GA20ox and inhibiting GA2ox expression (Penfield et al., 2006; Oh et al., 2007). The germination of seed imbibing in the cold is stimulated by increased GA levels, but cold acclimation of adult plants is associated with decreased GA. Induction of the C-repeat-binding factor genes by cold acclimation induces the GA turnover GA2ox genes (Achard et al., 2008). Decreased GA levels enhance cold tolerance and suppress plant growth in the cold. GA stimulates the transition from meristematic growth to shoot differentiation. KNOX genes maintain the meristem by repressing the GA biosynthesis GA20ox enzymes and activating the transcript accumulation of the GA turnover GA2ox enzymes (for review, see Galinha et al., 2009). GA20ox expression, and presumably GA accumulation, is high in new shoots but depleted in the meristem. The GA signal is perceived by a soluble receptor protein, GA-INSENSITIVE DWARF1 (GID1). The mechanisms of GA perception are conserved, showing agreement in Arabidopsis and rice, where the signaling pathway has been studied in the greatest detail (Table I). The GID1 gene was identified through map-based cloning of