A Quick Release Mechanism for Abscisic Acid
2006; Cell Press; Volume: 126; Issue: 6 Linguagem: Inglês
10.1016/j.cell.2006.09.001
ISSN1097-4172
AutoresJulian I. Schroeder, Eiji Nambara,
Tópico(s)Calcium signaling and nucleotide metabolism
ResumoThe hormone abscisic acid regulates development and survival of plants in response to environmental stresses. Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar now demonstrate that in response to stress, abscisic acid can be made available via polymerization of a β-glucosidase enzyme. This enzyme is reported to hydrolyze glucose-conjugated abscisic acid, thus increasing active abscisic acid concentrations. The hormone abscisic acid regulates development and survival of plants in response to environmental stresses. Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar now demonstrate that in response to stress, abscisic acid can be made available via polymerization of a β-glucosidase enzyme. This enzyme is reported to hydrolyze glucose-conjugated abscisic acid, thus increasing active abscisic acid concentrations. Plants are immobile and therefore need to cope effectively with environmental stresses. To this end, plants have a stress hormone, abscisic acid (ABA), that enables plants to survive recurring stresses such as drought, cold, and high salt in soils. Studies have indicated that ABA concentrations can be rapidly increased in response to these osmotic stresses. However, the mechanisms underlying this phenomenon have remained unclear. Previous research has shown that ABA can be conjugated with glucose, which represents an inactive pool of ABA (Dietz et al., 2000Dietz K.-J. Sauter A. Wichert K. Messdaghi D. Hartung W. J. Exp. Bot. 2000; 51: 937-944Crossref PubMed Google Scholar, Hartung et al., 2002Hartung W. Sauter A. Hose E. J. Exp. Bot. 2002; 53: 27-32Crossref PubMed Google Scholar, Nambara and Marion-Poll, 2005Nambara E. Marion-Poll A. Annu. Rev. Plant Biol. 2005; 56: 165-185Crossref PubMed Scopus (1411) Google Scholar). In this issue of Cell, Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar demonstrate that the cleavage of glucose-conjugated ABA by an ABA-specific β-glucosidase, AtBG1, is a new way to produce bioactive ABA in response to dehydration stress and also day/night conditions. Endogenous ABA levels increase when plants are subjected to osmotic stress and decrease when rescued from stressed conditions. These changes are regulated through the rate of ABA synthesis and ABA breakdown (Figure 1) (Nambara and Marion-Poll, 2005Nambara E. Marion-Poll A. Annu. Rev. Plant Biol. 2005; 56: 165-185Crossref PubMed Scopus (1411) Google Scholar). Xanthoxin synthesis catalyzed by 9-cis-epoxycarotenoid dioxygenases is known to be the rate-limiting step in de novo ABA synthesis, whereas ABA breakdown is mediated by the P450 proteins, named CYP707As, which results in production of phaseic acid as the breakdown product (Figure 1). ABA is also conjugated with glucose, resulting in formation of an ABA glucose ester (ABA-GE) (Figure 1). ABA-GE is one of the major inactive forms of ABA and is widespread in the plant kingdom (Hartung et al., 2002Hartung W. Sauter A. Hose E. J. Exp. Bot. 2002; 53: 27-32Crossref PubMed Google Scholar). Interestingly, repetitive cycles of dehydration/rehydration cause fluctuating accumulation patterns of phaseic acid but cause a stepwise increase in ABA-GE levels correlating with the number of cycles (Zeevaart, 1983Zeevaart J.A.D. Plant Physiol. 1983; 71: 477-481Crossref PubMed Google Scholar). It has remained unclear whether this accumulation of ABA-GE is merely a sign of stress history or a stored form of releasable ABA (Hartung et al., 2002Hartung W. Sauter A. Hose E. J. Exp. Bot. 2002; 53: 27-32Crossref PubMed Google Scholar). Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar reveal that ABA-GE can be hydrolyzed in response to stress by the β-glucosidase AtBG1, thus leading to an increase in the active ABA concentration. In addition to its role in stress responses, ABA also affects many developmental processes, including induction and maintenance of seed dormancy, thereby inhibiting seed germination. Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar report that loss of function of the atbg1 gene (that encodes a β-glucosidase) causes a reduction in the ABA concentration in seeds and concomitantly an earlier germination of seeds. ABA also mediates closing of stomatal pores in the surface of leaves in response to drought stress. Stomatal pores allow the influx of CO2 from the atmosphere into leaves, but at the same time these pores are the major conduits for plant water loss. Therefore, the closing of stomatal pores induced by ABA reduces water loss in plants. Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar show that overexpression of AtBG1 results in increased ABA concentrations, causing reduced water loss and enhanced drought resistance of plants, even in response to mild drought treatments (such as exposure of plate-grown plants to 30% humidity for 10 hr). The authors also report that stomatal closing induced by darkness is impaired in atbg1 loss-of-function mutant leaves (Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar), indicating that ABA production may be required for this response to darkness. On the other hand, Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar also report a reduction in whole leaf ABA concentration at night time during day/night cycles. It will be interesting to determine the cause for the apparent difference in ABA levels during darkness-induced stomatal closing and dark phases of day/night cycles. The authors further identify a mechanism by which stresses and day/night cycles regulate the ABA-GE glucosidase activity of AtBG1. Previous work has suggested that formation of active β-glucosidases requires polymerization of β-glucosidase monomers (Kim and Kim, 1998Kim Y.-W. Kim I.S. Biochim. Biophys. Acta. 1998; 1388: 457-464Crossref PubMed Scopus (13) Google Scholar). Interestingly both mild drought treatments and day/night cycles are shown to cause a progressive polymerization over time of the AtBG1 protein up to a final molecular weight of 600 kDa (AtBG1 monomer MW is ∼60 kDa) (Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar). Furthermore the high-molecular-weight complex showed an increase (>3-fold) in ABA-GE hydrolysis activity compared to the low-molecular-weight fraction (Figure 1). These findings could have implications for the local production of ABA, for example in leaves, during stress via hydrolysis of a pre-existing pool of inactive ABA-GE. A classical model has proposed that drought-stressed roots produce ABA, which is then transported to leaves via the xylem, as part of the "root-to-leaf" drought signal. However, Christmann et al., 2005Christmann A. Hoffmann T. Teplova I. Grill E. Müller A. Plant Physiol. 2005; 137: 209-219Crossref PubMed Scopus (190) Google Scholar examined the expression of reporters controlled by ABA-inducible promoters to noninvasively determine where and when ABA is produced in intact plants in response to drought stress of roots. This recent study provided evidence that ABA production occurs in leaves, leading to a new model in which a different signal than ABA transmits the drought stress response from roots to leaves, and this unknown "root-to-leaf" long-distance signal in turn causes ABA production in leaves (Christmann et al., 2005Christmann A. Hoffmann T. Teplova I. Grill E. Müller A. Plant Physiol. 2005; 137: 209-219Crossref PubMed Scopus (190) Google Scholar). Lowering the ambient humidity in the air surrounding leaves leads to a rapid partial closing of stomatal pores in leaves. A recent elegant genetic screen has isolated two mutants that are defective in this rapid stomatal closure induced by low humidity (Xie et al., 2006Xie X. Wang Y. Williamson L. Holroyd G.H. Tagliavia C. Murchie E. Theobald J. Knight M.R. Davies W.J. Leyser H.M.O. et al.Curr. Biol. 2006; 16: 882-887Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar). Interestingly, the two isolated mutant genes encode ABA biosynthesis (ABA2 short-chain dehydrogenase/reductase) and ABA signal transduction (OST1/SnRK2e protein kinase) components. This result led to the model that a rapid drop in humidity in air surrounding leaves results in a rapid increase in local ABA levels and thus stomatal closing. It will be interesting to determine whether the findings of these two recent studies (Christmann et al., 2005Christmann A. Hoffmann T. Teplova I. Grill E. Müller A. Plant Physiol. 2005; 137: 209-219Crossref PubMed Scopus (190) Google Scholar and Xie et al., 2006Xie X. Wang Y. Williamson L. Holroyd G.H. Tagliavia C. Murchie E. Theobald J. Knight M.R. Davies W.J. Leyser H.M.O. et al.Curr. Biol. 2006; 16: 882-887Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar) can at least in part be explained by AtBG1-mediated ABA production in leaves from conjugated ABA-GE. Consistent with such a model, cell type-specific microarray analyses of guard cells and mesophyll cells (Leonhardt et al., 2004Leonhardt N. Kwak J.M. Robert N. Waner D. Leonhardt G. Schroeder J.I. Plant Cell. 2004; 16: 596-615Crossref PubMed Scopus (439) Google Scholar) indicate guard cell expression and even higher mesophyll expression levels of AtBG1 mRNA. Current publicly available microarray data indicate that expression of AtBG1 is apparently very high in the shoot apex and in reproductive plant organs, implicating possible roles for AtBG1 in development or in stress responses to ABA in these tissues (Zimmermann et al., 2004Zimmermann P. Hirsch-Hoffmann M. Henning L. Gruissem W. Plant Physiol. 2004; 136: 2621-2632Crossref PubMed Scopus (1978) Google Scholar). ABA-GE is located in intracellular storage organelles (vacuoles), in xylem sap, and probably in the cytosol and cell wall as well (Dietz et al., 2000Dietz K.-J. Sauter A. Wichert K. Messdaghi D. Hartung W. J. Exp. Bot. 2000; 51: 937-944Crossref PubMed Google Scholar). Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar show that the AtBG1 β-glucosidase is located in the endoplasmic reticulum (ER) and remains in the ER during stress responses. Thus the authors propose that an important aspect of stress responses may be the activation of transporter proteins that shuttle ABA-GE into the ER. The authors further examined where AtBG1-dependent ABA accumulates in the cell. Using ELISA (enzyme-linked immunosorbent assays) and collection of different compartment fluids to quantify hormone levels, Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar report that ABA accumulation in the extracellular space is markedly reduced in atbg1 mutant plants. In contrast, no large differences were found in intracellular and xylem sap ABA concentrations between wild-type and atbg1 plants. Additional analyses using mass spectrometry techniques would allow the quantitation of ABA precursors and breakdown products, which could be useful to evaluate whether or not the classical pathway (i.e., de novo ABA synthesis) is also involved in the rapid increase in ABA levels. The cellular location of stress-related ABA receptors remains unknown. Studies in a number of laboratories have provided evidence for plasma membrane ABA receptors, but research in four different laboratories has also shown that guard cells respond to intracellular ABA (reviewed in Finkelstein and Rock, 2002Finkelstein R. Rock C. Abscisic acid biosynthesis and signaling.in: Somerville C.R. Meyerowitz E.M. The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD2002Google Scholar, Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar). Thus the relevance of extracellular ABA accumulation awaits further studies. The research of Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar supports a model in which ABA can be rapidly and locally released by AtBG1 through the posttranslational polymerization of the AtBG1 protein. These findings lead to several newly arising questions. How do environmental stresses cause polymerization of ABA-GE glucosidases? Does AtBG1 polymerization require protein modification or other cofactors? The findings of Lee et al., 2006Lee K.H. Kim H.-Y. Piao H.L. Choi S.M. Jiang F. Hartung W. Hwang I. Kwak J.M. Lee I.-J. Hwang I. Cell. 2006; (this issue)Google Scholar also indicate that uncharacterized transport systems are involved in the movement of ABA-GE and ABA. This study opens the door to investigations of new regulatory mechanisms that mediate plant hormone mobilization and sheds light into how plants adapt to environmental challenges. Activation of Glucosidase via Stress-Induced Polymerization Rapidly Increases Active Pools of Abscisic AcidLee et al.CellSeptember 22, 2006In BriefAbscisic acid (ABA) is a phytohormone critical for plant growth, development, and adaptation to various stress conditions. Plants have to adjust ABA levels constantly to respond to changing physiological and environmental conditions. To date, the mechanisms for fine-tuning ABA levels remain elusive. Here we report that AtBG1, a β-glucosidase, hydrolyzes glucose-conjugated, biologically inactive ABA to produce active ABA. Loss of AtBG1 causes defective stomatal movement, early germination, abiotic stress-sensitive phenotypes, and lower ABA levels, whereas plants with ectopic AtBG1 accumulate higher ABA levels and display enhanced tolerance to abiotic stress. 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