The control of transpiration. Insights from Arabidopsis.
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Arabidopsis↗
Biomedical subjects
Sarah M Assmann
Publications and source records attributed to Sarah M Assmann.
Light regulation of stomatal movement.
Stomatal pores, each surrounded by a pair of guard cells, regulate CO2 uptake and water loss from leaves. Stomatal opening is driven by the accumulation of K+ salts and sugars in guard cells, which is mediated by electrogenic proton pumps in the plasma membrane and/or metabolic activity. Opening responses are achieved by coordination of light signaling, light-energy conversion, membrane ion transport, and metabolic activity in guard cells. In this review, we focus on recent progress in blue- and red-light-dependent stomatal opening. Because the blue-light response of stomata appears to be strongly affected by red light, we discuss underlying mechanisms in the interaction between blue-light signaling and guard cell chloroplasts.
Abscisic Acid↗
G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development.
Abscisic acid (ABA) plays regulatory roles in a host of physiological processes throughout plant growth and development. Seed germination, early seedling development, stomatal guard cell functions, and acclimation to adverse environmental conditions are key processes regulated by ABA. Recent evidence suggests that signaling processes in both seeds and guard cells involve heterotrimeric G proteins. To assess new roles for the Arabidopsis (Arabidopsis thaliana) Galpha subunit (GPA1), the Gbeta subunit (AGB1), and the candidate G-protein-coupled receptor (GCR1) in ABA signaling during germination and early seedling development, we utilized knockout mutants lacking one or more of these components. Our data show that GPA1, AGB1, and GCR1 each negatively regulates ABA signaling in seed germination and early seedling development. Plants lacking AGB1 have greater ABA hypersensitivity than plants lacking GPA1, suggesting that AGB1 is the predominant regulator of ABA signaling and that GPA1 affects the efficacy of AGB1 execution. GCR1 acts upstream of GPA1 and AGB1 for ABA signaling pathways during germination and early seedling development: gcr1 gpa1 double mutants exhibit a gpa1 phenotype and agb1 gcr1 and agb1 gcr1 gpa1 mutants exhibit an agb1 phenotype. Contrary to the scenario in guard cells, where GCR1 and GPA1 have opposite effects on ABA signaling during stomatal opening, GCR1 acts in concert with GPA1 and AGB1 in ABA signaling during germination and early seedling development. Thus, cell- and tissue-specific functional interaction in response to a given signal such as ABA may determine the distinct pathways regulated by the individual members of the G-protein complex.
Abscisic Acid↗
Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling.
Plants both lose water and take in carbon dioxide through microscopic stomatal pores, each of which is regulated by a surrounding pair of guard cells. During drought, the plant hormone abscisic acid (ABA) inhibits stomatal opening and promotes stomatal closure, thereby promoting water conservation. Dozens of cellular components have been identified to function in ABA regulation of guard cell volume and thus of stomatal aperture, but a dynamic description is still not available for this complex process. Here we synthesize experimental results into a consistent guard cell signal transduction network for ABA-induced stomatal closure, and develop a dynamic model of this process. Our model captures the regulation of more than 40 identified network components, and accords well with previous experimental results at both the pathway and whole-cell physiological level. By simulating gene disruptions and pharmacological interventions we find that the network is robust against a significant fraction of possible perturbations. Our analysis reveals the novel predictions that the disruption of membrane depolarizability, anion efflux, actin cytoskeleton reorganization, cytosolic pH increase, the phosphatidic acid pathway, or K(+) efflux through slowly activating K(+) channels at the plasma membrane lead to the strongest reduction in ABA responsiveness. Initial experimental analysis assessing ABA-induced stomatal closure in the presence of cytosolic pH clamp imposed by the weak acid butyrate is consistent with model prediction. Simulations of stomatal response as derived from our model provide an efficient tool for the identification of candidate manipulations that have the best chance of conferring increased drought stress tolerance and for the prioritization of future wet bench analyses. Our method can be readily applied to other biological signaling networks to identify key regulatory components in systems where quantitative information is limited.
Abscisic Acid↗
G protein signaling in the regulation of rice seed germination.
Seed germination and early seedling growth are regulated by an intricate network of hormonal signaling pathways. The plant hormones gibberellic acid (GA) and abscisic acid (ABA) are particularly important positive and negative regulators of these processes, respectively. In the cereal rice, mutant analysis has implicated heterotrimeric guanine nucleotide-binding protein (G protein) signaling in GA-stimulated expression of several genes, including expression of the gene encoding the hydrolytic enzyme alpha-amylase, which breaks down carbohydrate reserves and thus mobilizes nutrients that nourish the young seedling.
Arabidopsis↗
G protein regulation of disease resistance during infection of rice with rice blast fungus.
When the effects of specific pathogen-produced elicitor compounds on plant cells are recognized by specific plant resistance (R) gene products, a local defense response called the hypersensitive response is triggered. Production of reactive oxygen species (ROS) and induction of defense genes are components of this response. In rice cultivars harboring null mutations in the G protein alpha subunit, RGA1, ROS production and defense gene induction by the rice blast fungus Magnaporthe grisea and its sphingolipid elicitors are reduced or delayed. These results implicate heterotrimeric guanine nucleotide-binding proteins (G proteins) as important players in plant pathogen response.
Apoptosis↗
G protein signaling in the regulation of Arabidopsis seed germination.
Seed germination and early seedling growth are regulated by an intricate network of hormonal signaling pathways. The plant hormones gibberellic acid (GA) and brassinosteroids (BRs) are important positive regulators of these processes, whereas the hormone abscisic acid (ABA) is a potent negative regulator. In Arabidopsis, analysis of mutant plants has implicated heterotrimeric guanine nucleotide-binding protein (G protein) components in regulation of seed germination by all three of these hormones.
Abscisic Acid↗
G proteins Go green: a plant G protein signaling FAQ sheet.
Plants, like animals, use signal transduction pathways based on heterotrimeric guanine nucleotide-binding proteins (G proteins) to regulate many aspects of development and cell signaling. Some components of G protein signaling are highly conserved between plants and animals and some are not. This Viewpoint compares key aspects of G protein signal transduction in plants and animals and describes the current knowledge of this system in plants, the questions that still await exploration, and the value of research on plant G proteins to scientists who do not study plants. Pathways in Science's Signal Transduction Knowledge Environment Connections Maps database provide details about the emerging roles of G proteins in several cellular processes of plants.
Animals↗
Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture.
Sphingolipids are a major component of membrane lipids and their metabolite sphingosine-1-phosphate (S1P) is a potent lipid mediator in animal cells. Recently, we have shown that the enzyme responsible for S1P production, sphingosine kinase (SphK), is stimulated by the phytohormone abscisic acid in guard cells of Arabidopsis (Arabidopsis thaliana) and that S1P is effective in regulating guard cell turgor. We have now characterized SphK from Arabidopsis leaves. SphK activity was mainly associated with the membrane fraction and phosphorylated predominantly the Delta4-unsaturated long-chain sphingoid bases sphingosine (Sph) and 4,8-sphingadienine, and to a lesser extent, the saturated long-chain sphingoid bases dihydrosphingosine and phytosphingosine (Phyto-Sph). 4-Hydroxy-8-sphingenine, which is a major sphingoid base in complex glycosphingolipids from Arabidopsis leaves, was a relatively poor substrate compared with the corresponding saturated Phyto-Sph. In contrast, mammalian SphK1 efficiently phosphorylated Sph, dihydrosphingosine, and 4,8-sphingadienine, but not the 4-hydroxylated long-chain bases Phyto-Sph and 4-hydroxy-8-sphingenine. Surface dilution kinetic analysis of Arabidopsis SphK with Sph presented in mixed Triton X-100 micelles indicated that SphK associates with the micellar surface and then with the substrate presented on the surface. In addition, measurements of SphK activity under different assay conditions combined with phylogenetic analysis suggest that multiple isoforms of SphK may be expressed in Arabidopsis. Importantly, we found that phytosphingosine-1-phosphate, similar to S1P, regulates stomatal apertures and that its action is impaired in guard cells of Arabidopsis plants harboring T-DNA null mutations in the sole prototypical G-protein alpha-subunit gene, GPA1.
Arabidopsis↗
Plant G proteins, phytohormones, and plasticity: three questions and a speculation.
Heterotrimeric guanine nucleotide-binding proteins (G proteins) composed of Galpha, Gbeta, and Ggamma subunits are important transducers of hormonal signals in organisms as evolutionarily distant as plants and humans. The genomes of diploid angiosperms, such as that of the model species Arabidopsis thaliana, encode only single canonical Galpha and Gbeta subunits, only two identified Ggamma subunits, and just one regulator of G protein signaling (RGS) protein. However, a wide range of processes-including seed germination, shoot and root growth, and stomatal regulation-are altered in Arabidopsis and rice plants with mutations in G protein components. Such mutants exhibit altered responsiveness to a number of plant hormones, including gibberellins, brassinosteroids, abscisic acid, and auxin. This review describes possible mechanisms by which such pleiotropic effects are generated and considers possible explanations for why G protein component mutations in plants fail to be lethal. A possible role of G protein signaling in the control of phenotypic plasticity, a hallmark of plant growth, is also discussed.
Animals↗
GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination.
Signal recognition by seven-transmembrane (7TM) cell-surface receptors is typically coupled by heterotrimeric G-proteins to downstream effectors in metazoan, fungal, and amoeboid cells. Some responses perceived by 7TM receptors in amoeboid cells and possibly in human cells can initiate downstream action independently of heterotrimeric G-proteins. Plants use heterotrimeric G-protein signaling in the regulation of growth and development, particularly in hormonal control of seed germination, but it is not yet clear which of these responses utilize a 7TM receptor. Arabidopsis GCR1 has a predicted 7TM-spanning domain and other features characteristic of 7TM receptors. Loss-of-function gcr1 mutants indicate that GCR1 plays a positive role in gibberellin- (GA) and brassinosteroid- (BR) regulated seed germination. The null mutants of GCR1 are less sensitive to GA and BR in seed germination. This phenotype is similar to that previously observed for transcript null mutants in the Galpha-subunit, gpa1. However, the reduced sensitivities toward GA and BR in the single gcr1, gpa1, and agb1 (heterotrimeric G-protein beta-subunit) mutants are additive or synergistic in the double and triple mutants. Thus, GCR1, unlike a typical 7TM receptor, apparently acts independently of the heterotrimeric G-protein in at least some aspects of seed germination, suggesting that this alternative mode of 7TM receptor action also functions in the plant kingdom.
Alleles↗
The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling.
Heterotrimeric G proteins composed of alpha, beta, and gamma subunits link ligand perception by G protein-coupled receptors (GPCRs) with downstream effectors, providing a ubiquitous signaling mechanism in eukaryotes. The Arabidopsis thaliana genome encodes single prototypical Galpha (GPA1) and Gbeta (AGB1) subunits, and two probable Ggamma subunits (AGG1 and AGG2). One Arabidopsis gene, GCR1, encodes a protein with significant sequence similarity to nonplant GPCRs and a predicted 7-transmembrane domain structure characteristic of GPCRs. However, whether GCR1 actually interacts with GPA1 was unknown. We demonstrate by in vitro pull-down assays, by yeast split-ubiquitin assays, and by coimmunoprecipitation from plant tissue that GCR1 and GPA1 are indeed physically coupled. GCR1-GPA1 interaction depends on intracellular domains of GCR1. gcr1 T-DNA insertional mutants exhibit hypersensitivity to abscisic acid (ABA) in assays of root growth, gene regulation, and stomatal response. gcr1 guard cells are also hypersensitive to the lipid metabolite, sphingosine-1-phosphate (S1P), which is a transducer of the ABA signal upstream of GPA1. Because gpa1 mutants exhibit insensitivity in aspects of guard cell ABA and S1P responses, whereas gcr1 mutants exhibit hypersensitivity, GCR1 may act as a negative regulator of GPA1-mediated ABA responses in guard cells.
Abscisic Acid↗
Guard cells: a dynamic signaling model.
The year 2003 has provided a continuing accretion of knowledge concerning the diverse ways in which guard cells sense and respond to abscisic acid. A deeper understanding of the biochemical mechanisms governing the response of guard cells to blue light has been gained, and new insights have been garnered regarding roles of the extracellular matrix in stomatal regulation.
Abscisic Acid↗
Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants.
Heterotrimeric G proteins have been implicated in a wide range of plant processes. These include responses to hormones, drought, and pathogens, and developmental events such as lateral root formation, hypocotyl elongation, hook opening, leaf expansion, and silique development. Results and concepts emerging from recent phenotypic analyses of G-protein component mutants in Arabidopsis and rice are adding to our understanding of G-protein mechanisms and functions in higher plants.
Alleles↗
Plants: the latest model system for G-protein research.
In humans, heterotrimeric G proteins couple stimulus perception by G-protein-coupled receptors (GPCRs) with numerous downstream effectors. By contrast, despite great complexity in their signal-transduction attributes, plants have a simpler repertoire of G-signalling components. Nonetheless, recent studies on Arabidopsis thaliana have shown the importance of plant G-protein signalling in such fundamental processes as cell proliferation, hormone perception and ion-channel regulation.
Cell Division↗
Abscisic acid induces rapid subnuclear reorganization in guard cells.
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Abscisic Acid↗
Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins.
In animals, the sphingolipid metabolite sphingosine-1-phosphate (S1P) functions as both an intracellular messenger and an extracellular ligand for G-protein-coupled receptors of the S1P receptor family, regulating diverse biological processes ranging from cell proliferation to apoptosis. Recently, it was discovered in plants that S1P is a signalling molecule involved in abscisic acid (ABA) regulation of guard cell turgor. Here we report that the enzyme responsible for S1P production, sphingosine kinase (SphK), is activated by ABA in Arabidopsis thaliana, and is involved in both ABA inhibition of stomatal opening and promotion of stomatal closure. Consistent with this observation, inhibition of SphK attenuates ABA regulation of guard cell inward K(+) channels and slow anion channels, which are involved in the regulation of stomatal pore size. Surprisingly, S1P regulates stomatal apertures and guard cell ion channel activities in wild-type plants, but not in knockout lines of the sole prototypical heterotrimeric G-protein alpha-subunit gene, GPA1 (refs 5, 6, 7-8). Our results implicate heterotrimeric G proteins as downstream elements in the S1P signalling pathway that mediates ABA regulation of stomatal function, and suggest that the interplay between S1P and heterotrimeric G proteins represents an evolutionarily conserved signalling mechanism.
Abscisic Acid↗
OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells.
The plant hormone abscisic acid plays a crucial role in plant responses to drought, salinity and cold. A recent report shows that mutations in the OST1 gene, encoding a serine-threonine protein kinase, render Arabidopsis thaliana guard cells insensitive to abscisic acid, such that stomata remain open in the presence of this phytohormone.
Abscisic Acid↗