Gibberellins (GAs) are plant hormones that regulate growth and influence various developmental processes, including stem elongation, germination, dormancy, flowering, sex expression, enzyme induction, and leaf and fruit senescence.
Gibberellin was first recognized in 1926 by a Japanese scientist, Eiichi Kurosawa, studying bakanae, the "foolish seedling" disease in rice. It was first isolated in 1935 by Teijiro Yabuta and Sumuki, from fungal strains (Gibberella fujikuroi) provided by Kurosawa. Yabuta named the isolate as gibberellin.
Interest in gibberellins outside of Japan began after World War II. In the United States, the first research was undertaken by a unit at Camp Detrick in Maryland, via studying seedlings of the bean Vicia faba. In the United Kingdom, work on isolating new types of gibberellin was undertaken at Imperial Chemical Industries. Interest in gibberellins spread around the world as the potential for its use on various commercially important plants became more obvious. For example, research that started at the University of California, Davis in the mid-1960s led to its commercial use on Thompson seedless table grapes throughout California by 1962. A known antagonist to gibberellin is paclobutrazol (PBZ), which in turn inhibits growth and induces early fruitset as well as seedset.
- 1 Chemistry
- 2 Bioactive GAs
- 3 Biological function
- 4 Biosynthesis
- 5 Gibberellin metabolism genes
- 6 Deactivation
- 7 Regulation
- 8 Gibberellin homeostasis
- 9 Impact on the “Green Revolution”
- 10 Receptors
- 11 Gibberellin and DELLA proteins
- 12 References
All known gibberellins are diterpenoid acids that are synthesized by the terpenoid pathway in plastids and then modified in the endoplasmic reticulum and cytosol until they reach their biologically-active form. All gibberellins are derived via the ent-gibberellane skeleton, but are synthesised via ent-kaurene. The gibberellins are named GA1 through GAn in order of discovery. Gibberellic acid, which was the first gibberellin to be structurally characterized, is GA3.
As of 2003, there were 126 GAs identified from plants, fungi, and bacteria.
Gibberellins are tetracyclic diterpene acids. There are two classes based on the presence of either 19 or 20 carbons. The 19-carbon gibberellins, such as gibberellic acid, have lost carbon 20 and, in place, possess a five-member lactone bridge that links carbons 4 and 10. The 19-carbon forms are, in general, the biologically active forms of gibberellins. Hydroxylation also has a great effect on the biological activity of the gibberellin. In general, the most biologically active compounds are dihydroxylated gibberellins, which possess hydroxyl groups on both carbon 3 and carbon 13. Gibberellic acid is a dihydroxylated gibberellin.
The bioactive GAs are GA1, GA3, GA4, and GA7. There are three common structural traits between these GAs: 1) a hydroxyl group on C-3β, 2) a carboxyl group on C-6, and 3) a lactone between C-4 and C-10. The 3β-hydroxyl group can be exchanged for other functional groups at C-2 and/or C-3 positions. GA5 and GA6 are examples of bioactive GAs that do not have a hydroxyl group on C-3β. The presence of GA1 in various plant species suggests that it is a common bioactive GA.
Gibberellins are involved in the natural process of breaking dormancy and various other aspects of germination. Before the photosynthetic apparatus develops sufficiently in the early stages of germination, the stored energy reserves of starch nourish the seedling. Usually in germination, the breakdown of starch to glucose in the endosperm begins shortly after the seed is exposed to water. Gibberellins in the seed embryo are believed to signal starch hydrolysis through inducing the synthesis of the enzyme α-amylase in the aleurone cells. In the model for gibberellin-induced production of α-amylase, it is demonstrated that gibberellins (denoted by GA) produced in the scutellum diffuse to the aleurone cells, where they stimulate the secretion α-amylase. α-Amylase then hydrolyses starch, which is abundant in many seeds, into glucose that can be used in cellular respiration to produce energy for the seed embryo. Studies of this process have indicated gibberellins cause higher levels of transcription of the gene coding for the α-amylase enzyme, to stimulate the synthesis of α-amylase.
Gibberellins are produced in greater mass when the plant is exposed to cold temperatures. They stimulate cell elongation, breaking and budding, seedless fruits, and seed germination. They do the last by breaking the seed’s dormancy and acting as a chemical messenger. Its hormone binds to a receptor, and Ca2+ activates the protein calmodulin, and the complex binds to DNA, producing an enzyme to stimulate growth in the embryo.
A major effect of gibberellins is the degradation of DELLA proteins, the absence of which then allows phytochrome interacting factors to bind to gene promoters and regulate gene expression. Gibberellins are thought to cause DELLAs to become polyubiquitinated and, thus, destroyed by the 26S proteasome pathway.
GAs are usually produced from the methylerythritol phosphate (MEP) pathway in higher plants. In this pathway, bioactive GA is produced from trans-geranylgeranyl diphosphate (GGDP). In the MEP pathway, three classes of enzymes are used to yield GA from GGDP: 1) terpene synthases (TPSs), 2) cytochrome P450 monooxygenases (P450s), and 3) 2-oxoglutarate–dependent dioxygenases (2ODDs). There are 8 steps in the methylerythritol phosphate pathway: - 1) GGDP is converted to ent-copalyl diphosphate (ent-CPD) by ent-copalyl diphosphate synthase - 2) etn-CDP is converted to ent-kaurene by ent-kaurene synthase - 3) ent-kaurene is converted to ent-kaurenol by ent-kaurene oxidase (KO) - 4) ent-kaurenol is converted to ent-kaurenal by KO - 5) ent-kaurenal is converted to ent-kaurenoic acid by KO - 6) ent-kaurenoic acid is converted to ent-7a-hydroxykaurenoic acid by ent-kaurene acid oxidase (KAO) - 7) ent-7a-hydroxykaurenoic acid is converted to GA12-aldehyde by KAO - 8) GA12-aldehyde is converted to GA12 by KAO. GA12 is processed to the bioactive GA4 by oxidations on C-20 and C-3, which is accomplished by 2 soluble ODDs: GA 20-oxidase and GA 3-oxidase.
Sites of biosynthesis
Most bioactive GAs are located in actively growing organs on plants. Both GA20ox and GA3ox genes (genes coding for GA 20-oxidase and GA 3-oxidase) and the SLENDER1 gene (a GA signal transduction gene) are found in growing organs on rice, which suggests bioactive GA synthesis occurs at their site of action in growing organs in plants. During flower development, the tapetum of anthers is believed to a primary site of GA biosynthesis.
Differences between biosynthesis in fungi and lower plants
Arabidopsis, a plant, and Gibberella fujikuroi, a fungus, possess different GA pathways and enzymes. P450s in fungi perform functions analogous to the functions of KAOs in plants. The function of CPS and KS in plants is performed by a single enzyme, CPS/KS, in fungi. In fungi, the GA biosynthesis genes are found on one chromosome, but in plants, they are found randomly on multiple chromosomes.
Gibberellin metabolism genes
One or two genes encode the enzymes responsible for the first steps of GA biosynthesis in Arabidopsis and rice. The null alleles of the genes encoding CPS, KS, and KO result in GA-deficient Arabidopsis dwarves. Multigene families encode the 2ODDs that catalyze the formation of GA12 to bioactive GA4.
AtGA3ox1 and AtGA3ox2, two of the four genes that encode GA3ox in Arabidopsis, affect vegetative development. Environmental stimuli regulate AtGA3ox1 and AtGA3ox2 activity during seed germination. In Arabidopsis, GA20ox overexpression leads to an increase in GA concentration.
Several mechanisms for inactivating GAs have been identified. 2β-hydroxylation deactivates GA, and is catalyzed by GA2-oxidases (GA2oxs). Some GA2oxs use C19-GAs as substrates, and other GA2oxs use C20-GAs.
Cytochrome P450 mono-oxygenase, encoded by elongated uppermost internode (eui), converts GAs into 16α,17-epoxides. Rice eui mutants amass bioactive GAs at high levels, which suggests cytochrome P450 mono-oxygenase is a main enzyme responsible for deactivation GA in rice.
Regulation by other hormones
The auxin indole-3-acetic acid (IAA) regulates concentration of GA1 in elongating internodes in peas. Removal of IAA by removal of the apical bud, the auxin source, reduces the concentration of GA1, and reintroduction of IAA reverses these effects to increase the concentration of GA1. This phenomenon has also been observed in tobacco plants. Auxin increases GA 3-oxidation and decreases GA 2-oxidation in barley. Auxin also regulates GA biosynthesis during fruit development in peas. These discoveries in different plant species suggest the auxin regulation of GA metabolism may be a universal mechanism.
Ethylene decreasing the concentration of bioactive GAs.
Regulation by environmental factors
Recent evidence suggests fluctuations in GA concentration influence light-regulated seed germination, photomorphogenesis during de-etiolation, and photoperiod regulation of stem elongation and flowering. Microarray analysis showed about one fourth cold-responsive genes are related to GA-regulated genes, which suggests GA influences response to cold temperatures. Plants reduce growth rate when exposed to stress. A relationship between GA levels and amount of stress experienced has been suggested in barley.
Role in seed development
Bioactive GAs and abcisic acid levels have an inverse relationship and regulate seed development and germination. Levels of FUS3, an Arabidopsis transcription factor, are upregulated by ABA and downregulated by GA, which suggests that there is a regulation loop that establishes the balance of GA and ABA.
Feedback and feedforward regulation maintains the levels of bioactive GAs in plants. Levels of AtGA20ox1 and AtGA3ox1 expression are increased in a GA deficient environment, and decreased after the addition of bioactive GAs, Conversely, expression of AtGA2ox1 and AtGA2ox2, GA deactivation genes, is increased with addition of GA.
Impact on the “Green Revolution”
A chronic food shortage was feared during the rapid climb in world population in the 1960s. This was averted with the development of a high-yielding variety of rice. This variety of semi-dwarf rice is called IR8, and it has a short height because of a mutation in the sd1 gene. Sd1 encodes GA20ox, so a mutant sd1 is expected to exhibit a short height that is consistent with GA deficiency.
GA receptors must have four traits: 1) reversibly bind GA, 2) GA saturability 3) high affinity for bioactive GA, and 4) reasonable ligand specificity for bioactive GAs.
Cereal aleurone cells
The first reported GA-binding protein (GBP) activity was discovered in wheat seed aleurone homogenates by using the GA-dependent induction of aleuron hydrolytic enzymes. Alpha-amylase induction in aleurone protoplasts is dependent on GA levels, but induction can still occur if GA does not pass through the plasma membrane. The existence of GA perception outside the cell and a plasma membrane GA receptor in aleurone cells can be concluded from these observations. Trimeric G proteins are involved in GA signaling, which supports the previous theory for plasma membrane GA receptors. Four different GBPs have been discovered in the plasma membrane of aleuron cells. Cereal aleurone cells could be unique in GA perception because they are some of the few plant cells that cannot synthesize bioactive GA.
The rice GID1 gene encodes an unknown protein that only has a high affinity for bioactive GAs. In yeast, GID1 binds SLR1, GA signaling repressor, depending on GA levels. GID1 is a soluble GA receptor mediating GA signaling. The GA-GID1 complex interacts with SLR1 to transduce the GA signal to SLR1. SLR1 increased the GA-binging activity of GID1 threefold. Arabidopsis has three GID1 homologs that bind GA and interact with DELLAs: AtGID1a, b, and c.
Gibberellin and DELLA proteins
DELLA proteins: repressors of GA-dependent processes
DELLA proteins act as intracellular repressors of GA responses, DELLAs inhibit seed germination, seed growth, and other GA-dependent pathways, but GA can reverse these effects.
For GA to bind to the GID1 receptor, the C3-hydroxyl on GA must form a hydrogen bond to the tyrosine 31 residue of GID1, which induces a conformational change in GID1 to enclose GA. Once GA is trapped in the GID1 pocket, the lid of the pocket binds to DELLA to form the GA-GID1-DELLA complex.
GA promotes proteasome-dependent degradation of DELLAs
In the absence of GA, many DELLAs are present to repress GA responses, but the formation of the GA-GID1-DELLA complex increases the degradation of DELLAs. The SCF complex is composed of SKP1, CULLIN, and F-BOX proteins. F-box proteins catalyze the formation of polyubiquitin on target proteins to be degraded by the 26S proteasome. The formation of the GA-GID1-DELLA complex is believed to cause a conformational change in DELLA, which enhances recognition of DELLAs by F-box proteins. Next, the SCF complex promotes ubiquitylation of DELLAs, which are then degraded by the 26S proteasome. Degradation of DELLAs allows GA regulated growth to resume. Thus, GA stimulates growth by activating the degradation of DELLAs.
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