Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution

Angiosperms (flowering plants) evolved relatively recently and are substantially diverged from early land plants (bryophytes, lycophytes, and others [1]). The phytohormone gibberellin (GA) adaptively regulates angiosperm growth via the GA-DELLA signaling mechanism [2-7]. GA binds to GA receptors (GID1s), thus stimulating interactions between GID1s and the growth-repressing DELLAs [8-12]. Subsequent 26S proteasome-mediated destruction of the DELLAs promotes growth [13-17]. Here we outline the evolution of the GA-DELLA mechanism. We show that the interaction between GID1 and DELLA components from Selaginella kraussiana (a lycophyte) is GA stimulated. In contrast, GID1-like (GLP1) and DELLA components from Physcomitrella patens (a bryophyte) do not interact, suggesting that GA-stimulated GID1-DELLA interactions arose in the land-plant lineage after the bryophyte divergence ( approximately 430 million years ago [1]). We further show that a DELLA-deficient P. patens mutant strain lacks the derepressed growth characteristic of DELLA-deficient angiosperms, and that both S. kraussiana and P. patens lack detectable growth responses to GA. These observations indicate that early land-plant DELLAs do not repress growth in situ. However, S. kraussiana and P. patens DELLAs function as growth-repressors when expressed in the angiosperm Arabidopsis thaliana. We conclude that the GA-DELLA growth-regulatory mechanism arose during land-plant evolution and via independent stepwise recruitment of GA-stimulated GID1-DELLA interaction and DELLA growth-repression functions.     

DELLA蛋白在被子植物有性生殖中的作用

DELLA蛋白是植物生长发育过程中响应赤霉素(GA)应答途径的关键调控因子, 主要行使转录调控因子的功能, 几乎参与了植物生长发育的各个重要过程。已有的研究表明, DELLA蛋白在被子植物的雄性生殖器官、雌性生殖器官和胚胎等组织中均有表达, 在植物有性生殖过程中起着极其重要的作用。该文综述了DELLA蛋白的分子结构、特性及其在植物有性生殖过程中的表达与功能, 并讨论了现存的问题及研究思路。     

The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants

Bioactive gibberellins (GAs) are diterpene phytohormones that modulate growth and development throughout the whole life cycle of the flowering plant. Impressive advances have been made in elucidating the GA pathway with the cloning and characterization of genes encoding most GA biosynthesis and catabolism enzymes, GA receptors (GIBBERELLIN INSENSITIVE DWARF1, GID1) and early GA signaling components. Recent biochemical, genetic and structural analyses demonstrate that GA de-represses its signaling pathway by GID1-induced degradation of DELLA proteins, which are master growth repressors, via a ubiquitin-proteasome pathway. Multiple endogenous signals and environmental cues also interact with the GA-GID1-DELLA regulatory module by affecting the expression of GA metabolism genes, and hence GA content and DELLA levels. Importantly, DELLA integrates different signaling activities by direct protein-protein interaction with multiple key regulatory proteins from other pathways. Comparative studies suggest that the functional GA-GID1-DELLA module is highly conserved among vascular plants, but not in the bryophytes. Interestingly, differentiation of the moss Physcomitrella patens is regulated by as yet unidentified ent-kaurene-derived diterpenes, which are distinct from the common active GAs in vascular plants.     

GA action: turning on de-DELLA repressing signaling

Phytohormone gibberellins (GA) are a large family of tetracyclic diterpenoids and play the important roles in modulation of plant growth and development throughout the plant life cycle. GA depresses its signaling by the GA-promoted destabilization of the DELLA protein growth repressors via 26S proteasome pathway. Recent evidences indicate that the DELLA proteins interact with multiple environmental and other hormonal response pathways and confer plant growth restraint. Furthermore, the discovery of rice GIBBERELLIN INSENSITIVE DWARF1 (GID1) and three Arabidopsis AtGID1 homologs as soluble GA receptors opens new prospects for understanding of de-DELLA repressing system in GA signaling.     

DELLA蛋白参与拟南芥幼苗对一氧化氮逆境的抵抗

DELLA蛋白是赤霉素信号途径中的一类对植物生长起抑制作用的重要蛋白质,在拟南芥（Arabidopsis thaliana）基因组中已经鉴定出5个DELLA蛋白基因。目前研究发现,DELLA蛋白在抗逆中也起了重要的作用。近年来,一氧化氮（nitric oxide,NO）的研究工作取得重要进展,低浓度的NO能够促进植物的生长,但在高浓度下它对植物生长起抑制作用甚至导致细胞死亡。通过外施一氧化氮供体硝普钠（sodium nitro prusside,SNP）,研究高浓度NO对拟南芥幼苗生长的影响,发现植物体内H2O2积累,幼苗死亡。通过研究DELLA蛋白基因表达的变化及其相关突变体的表型,证明DELLA蛋白在抵抗NO逆境中起了重要作用。研究结果揭示了DELLA蛋白与NO逆境的关系,为今后科学指导农业生产提供了理论依据。     

FKF1 F-box protein promotes flowering in part by negatively regulating DELLA protein stability under long-day photoperiod in Arabidopsis

FLAVIN‐BINDING KELCH REPEAT F‐BOX 1 (FKF1) encodes an F‐box protein that regulates photoperiod flowering in Arabidopsis under long‐day conditions (LDs). Gibberellin (GA) is also important for regulating flowering under LDs. However, how FKF1 and the GA pathway work in concert in regulating flowering is not fully understood. Here, we showed that the mutation of FKF1 could cause accumulation of DELLA proteins, which are crucial repressors in GA signaling pathway, thereby reducing plant sensitivity to GA in flowering. Both in vitro and in vivo biochemical analyses demonstrated that FKF1 directly interacted with DELLA proteins. Furthermore, we showed that FKF1 promoted ubiquitination and degradation of DELLA proteins. Analysis of genetic data revealed that FKF1 acted partially through DELLAs to regulate flowering under LDs. In addition, DELLAs exerted a negative feedback on FKF1 expression. Collectively, these findings demonstrate that FKF1 promotes flowering partially by negatively regulating DELLA protein stability under LDs, and suggesting a potential mechanism linking the FKF1 to the GA signaling DELLA proteins.     

Gibberellin biosynthesis and the regulation of plant development

Gibberellins (GAs) form a large family of plant growth substances with distinct functions during the whole life cycle of higher plants. The rate of GA biosynthesis and catabolism determines how the GA hormone pool occurs in plants in a tissue and developmentally regulated manner. With the availability of genes coding for GA biosynthetic enzymes, our understanding has improved dramatically of how GA plant hormones regulate and integrate a wide range of growth and developmental processes. This review focuses on two plant systems, pumpkin and Arabidopsis, which have added significantly to our understanding of GA biosynthesis and its regulation. In addition, we present models for regulation of GA biosynthesis in transgenic plants, and discuss their suitability for altering plant growth and development.     

Role of the gibberellin receptors GID1 during fruit‐set in Arabidopsis

Gibberellins (GAs) play a critical role in fruit‐set and fruit growth. Gibberellin is perceived by its nuclear receptors GA INSENSITIVE DWARF1s (GID1s), which then trigger degradation of downstream repressors DELLAs. To understand the role of the three GA receptor genes (GID1A, GID1B and GID1C) in Arabidopsis during fruit initiation, we have examined their temporal and spatial localization, in combination with analysis of mutant phenotypes. Distinct expression patterns are revealed for each GID1: GID1A is expressed throughout the whole pistil, while GID1B is expressed in ovules, and GID1C is expressed in valves. Functional study of gid1 mutant combinations confirms that GID1A plays a major role during fruit‐set and growth, whereas GID1B and GID1C have specific roles in seed development and pod elongation, respectively. Therefore, in ovules, GA perception is mediated by GID1A and GID1B, while GID1A and GID1C are involved in GA perception in valves. To identify tissue‐specific interactions between GID1s and DELLAs, we analyzed spatial expression patterns of four DELLA genes that have a role in fruit initiation (GAI, RGA, RGL1 and RGL2). Our data suggest that GID1A can interact with RGA and GAI in all tissues, whereas GID1C–RGL1 and GID1B–RGL2 interactions only occur in valves and ovules, respectively. These results uncover specific functions of each GID1–DELLA in the different GA‐dependent processes that occur upon fruit‐set. In addition, the distribution of GA receptors in valves along with lack of expression of GA biosynthesis genes in this tissue, strongly suggests transport of GAs from the developing seeds to promote fruit growth.