The ABA receptors -- we report you decide

The plant hormone abscisic acid (ABA) has been implicated in a variety of physiological responses ranging from seed dormancy to stomatal conductance. Recently, three groups have reported the molecular identification of three disparate ABA receptors. Unlike the identification of other hormone receptors, in these three cases high affinity binding to ABA rather than the isolation of ABA insensitive mutants led to these receptor genes. Interestingly, two of the receptors encode genes involved in floral timing and chlorophyll biosynthesis, which are not considered traditional ABA responses. And the third receptor has been clouded in issues of its molecular identity. To clearly determine the roles of these genes in ABA perception it will require placing of these ABA-binding proteins into the rich ABA physiological context that has built up over the years.     

Hormone signalling from a developmental context

The influence of hormones on plant growth and development has been clearly documented over the past 50 years. Now, with molecular genetics, the genes that convert changes in hormone levels into a cellular response are beginning to be identified. However, recent studies have demonstrated that the developmental context in which the hormones act plays a large influence on their synthesis and action. In this review, examples are given where known hormone response genes have been shown to have broader developmental roles as well as examples where genes that regulate developmental decisions, such as differentiation and fate, also influence hormone metabolism. The early conclusion of these studies is that an understanding of hormone signal transduction cannot be achieved in the absence of a developmental framework.     

Early ABA Signaling Events in Guard Cells

The plant hormone abscisic acid (ABA) regulates a wide variety of plant physiological and developmental processes, particularly responses to environmental stress, such as drought. In response to water deficiency, plants redistribute foliar ABA and/or upregulate ABA synthesis in roots, leading to roughly a 30-fold increase in ABA concentration in the apoplast of stomatal guard cells. The elevated ABA triggers a chain of events in guard cells, causing stomatal closure and thus preventing water loss. Although the molecular nature of ABA receptor(s) remains unknown, considerable progress in the identification and characterization of its downstream signaling elements has been made by using combined physiological, biochemical, biophysical, molecular, and genetic approaches. The measurable events associated with ABA-induced stomatal closure in guard cells include, sequentially, the production of reactive oxygen species (ROS), increases in cytosolic free Ca²⁺ levels ([Ca²⁺]_i), activation of anion channels, membrane potential depolarization, cytosolic alkalinization, inhibition of K⁺ influx channels, and promotion of K⁺ efflux channels. This review provides an overview of the cellular and molecular mechanisms underlying these ABA-evoked signaling events, with particular emphasis on how ABA triggers an “electronic circuitry” involving these ionic components.     

Hormonal input in plant meristems: A balancing act

Plant hormones are a group of chemically diverse molecules that control virtually all aspects of plant development. Classical plant hormones were identified many decades ago in physiology studies that addressed plant growth regulation. In recent years, biochemical and genetic approaches led to the identification of many molecular components that mediate hormone activity, such as hormone receptors and hormone-regulated genes. This has greatly contributed to the understanding of the mechanisms underlying hormone activity and highlighted the intricate crosstalk and integration of hormone signalling and developmental pathways. Here we review and discuss recent findings on how hormones regulate the activity of shoot and root apical meristems.     

Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease

We have found that a major target for effectors secreted by Pseudomonas syringae is the abscisic acid (ABA) signalling pathway. Microarray data identified a prominent group of effector-induced genes that were associated with ABA biosynthesis and also responses to this plant hormone. Genes upregulated by effector delivery share a 42% overlap with ABA-responsive genes and are also components of networks induced by osmotic stress and drought. Strongly induced were NCED3, encoding a key enzyme of ABA biosynthesis, and the abscisic acid insensitive 1 (ABI1) clade of genes encoding protein phosphatases type 2C (PP2Cs) involved in the regulation of ABA signalling. Modification of PP2C expression resulting in ABA insensitivity or hypersensitivity led to restriction or enhanced multiplication of bacteria, respectively. Levels of ABA increased rapidly during bacterial colonisation. Exogenous ABA application enhanced susceptibility, whereas colonisation was reduced in an ABA biosynthetic mutant. Expression of the bacterial effector AvrPtoB in planta modified host ABA signalling. Our data suggest that a major virulence strategy is effector-mediated manipulation of plant hormone homeostasis, which leads to the suppression of defence responses.     

Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis

Although abscisic acid (ABA) is involved in a variety of plant growth and developmental processes, few genes that actually regulate the transduction of the ABA signal into a cellular response have been identified. In an attempt to determine negative regulators of ABA signaling, we identified mutants, designated enhanced response to ABA3 (era3), that increased the sensitivity of the seed to ABA. Biochemical and molecular analyses demonstrated that era3 mutants overaccumulate ABA, suggesting that era3 is a negative regulator of ABA synthesis. Subsequent genetic analysis of era3 alleles, however, showed that these are new alleles at the ETHYLENE INSENSITIVE2 locus. Other mutants defective in their response to ethylene also showed altered ABA sensitivity; from these results, we conclude that ethylene appears to be a negative regulator of ABA action during germination. In contrast, the ethylene response pathway positively regulates some aspects of ABA action that involve root growth in the absence of ethylene. We discuss the response of plants to ethylene and ABA in the context of how these two hormones could influence the same growth responses.     

A protein phosphatase 2A catalytic subunit is a negative regulator of abscisic acid signalling

The key regulatory role of abscisic acid (ABA) in many physiological processes in plants is well established. However, compared with other plant hormones, the molecular mechanisms underlying ABA signalling are poorly characterized. In this work, a specific catalytic subunit of protein phosphatase 2A (PP2Ac-2) has been identified as a component of the signalling pathway that represses responses to ABA. A loss-of-function pp2ac-2 mutant is hypersensitive to ABA. Moreover, pp2ac-2 plants have altered responses in developmental and environmental processes that are mediated by ABA, such as primary and lateral root development, seed germination and responses to drought and high salt and sugar stresses. Conversely, transgenic plants overexpressing PP2Ac-2 are less sensitive to ABA than wild type, a phenotype that is manifested in all the above-mentioned physiological processes. DNA microarray hybridization experiments reveal that PP2Ac-2 is negatively involved in ABA responses through regulation of ABA-dependent gene expression. Moreover, the results obtained indicate that ABA antagonistically regulates PP2Ac-2 expression and PP2Ac-2 activity thus allowing plant sensitivity to the hormone to be reset after induction. Phenotypic, genetic and gene expression data strongly suggest that PP2Ac-2 is a negative regulator of the ABA pathway. Activity of protein phosphatase 2A thus emerges as a key element in the control of ABA signalling.     

From common signalling components to cell specific responses: insights from the cereal aleurone

Studies into the molecules underlying plant signal transduction events continue to reveal the involvement of highly conserved factors such as Ca²⁺, calmodulin, cyclic GMP and phospholipases in a remarkably diverse array of physiological processes. The hormonal response systems in the aleurone cells of the cereal grain and in the stomatal guard cell are beginning to reveal how diversity of response can be hard wired into these cells despite the use of these common signalling intermediates. In both the aleurone and the guard cell ABA signalling operates through the action of phospholipase D and alterations in a Ca²⁺-dependent signalling system. The role of phospholipase D is highly analogous in these two divergent cell types, perhaps reflecting the closeness of this enzyme to a conserved ABA receptor. However, specificity in response becomes evident in elements downstream from PLD, such as in the Ca²⁺ signalling system. For example, ABA has opposite effects on cytoplasmic Ca²⁺ in the aleurone and guard cell. Combining the Ca²⁺-dependent signalling activities in networks with parallel regulatory activities such as cyclic GMP appears to underlie the flexible regulatory systems that are the hallmark of plant cell function.     

Towards mechanistic models of plant organ growth

Modelling and simulation are increasingly used as tools in the study of plant growth and developmental processes. By formulating experimentally obtained knowledge as a system of interacting mathematical equations, it becomes feasible for biologists to gain a mechanistic understanding of the complex behaviour of biological systems. In this review, the modelling tools that are currently available and the progress that has been made to model plant development, based on experimental knowledge, are described. In terms of implementation, it is argued that, for the modelling of plant organ growth, the cellular level should form the cornerstone. It integrates the output of molecular regulatory networks to two processes, cell division and cell expansion, that drive growth and development of the organ. In turn, these cellular processes are controlled at the molecular level by hormone signalling. Therefore, combining a cellular modelling framework with regulatory modules for the regulation of cell division, expansion, and hormone signalling could form the basis of a functional organ growth simulation model. The current state of progress towards this aim is that the regulation of the cell cycle and hormone transport have been modelled extensively and these modules could be integrated. However, much less progress has been made on the modelling of cell expansion, which urgently needs to be addressed. A limitation of the current generation models is that they are largely qualitative. The possibilities to characterize existing and future models more quantitatively will be discussed. Together with experimental methods to measure crucial model parameters, these modelling techniques provide a basis to develop a Systems Biology approach to gain a fundamental insight into the relationship between gene function and whole organ behaviour.     

Plant hormone mutants

The techniques used for the production and identification of plant hormone mutants are described. The properties used to classify these mutants into the broad synthesis and response categories are discussed, and the genetic considerations needed to allow their effective use in plant hormone research examined. A brief outline of significant work on gibberellin (GA), abscisic acid (ABA), auxin, ethylene, cytokinin and phytochrome mutants is provided. The molecular action of these genes is discussed where available and recent rapid advances made in Arabidopsis highlighted. Suggestions for future emphasis are made, particularly relating to an examination of the tissue and ontogenetic specificity of the plant hormone genes.     

A thermodynamic switch modulates abscisic acid receptor sensitivity

Abscisic acid (ABA) is a key hormone regulating plant growth, development and the response to biotic and abiotic stress. ABA binding to pyrabactin resistance (PYR)/PYR1-like (PYL)/Regulatory Component of Abscisic acid Receptor (RCAR) intracellular receptors promotes the formation of stable complexes with certain protein phosphatases type 2C (PP2Cs), leading to the activation of ABA signalling. The PYR/PYL/RCAR family contains 14 genes in Arabidopsis and is currently the largest plant hormone receptor family known; however, it is unclear what functional differentiation exists among receptors. Here, we identify two distinct classes of receptors, dimeric and monomeric, with different intrinsic affinities for ABA and whose differential properties are determined by the oligomeric state of their apo forms. Moreover, we find a residue in PYR1, H60, that is variable between family members and plays a key role in determining oligomeric state. In silico modelling of the ABA activation pathway reveals that monomeric receptors have a competitive advantage for binding to ABA and PP2Cs. This work illustrates how receptor oligomerization can modulate hormonal responses and more generally, the sensitivity of a ligand-dependent signalling system.     

Pathological hormone imbalances

Plant hormones play important roles in regulating developmental processes and signalling networks involved in plant responses to a wide range of biotic and abiotic stresses. Salicylic acid (SA), jasmonates (JA) and ethylene (ET) are well known to play crucial roles in plant disease and pest resistance. However, the roles of other hormones such as abscisic acid (ABA), auxin, gibberellin (GA), cytokinin (CK) and brassinosteroid (BL) in plant defence are less well known. Much progress has been made in understanding plant hormone signalling and plant disease resistance. However, these studies have mostly proceeded independently of each other, and there is limited knowledge regarding interactions between plant hormone-mediated signalling and responses to various pathogens. Here, we review the roles of hormones other than SA, JA and ET in plant defence and the interactions between hormone-mediated signalling, plant defence and pathogen virulence. We propose that these hormones may influence disease outcomes through their effect on SA or JA signalling.     

Decoding ABA and osmostress signalling in plants from an evolutionary point of view

The plant hormone abscisic acid (ABA) is fundamental for land plant adaptation to water-limited conditions. Osmostress, such as drought, induces ABA accumulation in angiosperms, triggering physiological responses such as stomata closure. The core components of angiosperm ABA signalling are soluble ABA receptors, group A protein phosphatase type 2C and SNF1-related protein kinase2 (SnRK2). ABA also has various functions in non-angiosperms, however, suggesting that its role in adaptation to land may not have been angiosperm-specific. Indeed, among land plants, the core ABA signalling components are evolutionarily conserved, implying their presence in a common ancestor. Results of ongoing functional genomics studies of ABA signalling components in bryophytes and algae have expanded our understanding of the evolutionary role of ABA signalling, with genome sequencing uncovering the ABA core module even in algae. In this review, we describe recent discoveries involving the ABA core module in non-angiosperms, tracing the footprints of how ABA evolved as a phytohormone. We also cover the latest findings on Raf-like kinases as upstream regulators of the core ABA module component SnRK2. Finally, we discuss the origin of ABA signalling from an evolutionary perspective.