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Update TRENDS in Plant Science 6 Steffenson, B.J. (1992) Analysis of durable resistance to stem rust in barley. Euphytica 63, 153 – 167 7 Brueggeman, R. et al. (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. U. S. A. 99, 9328 – 9333 8 Horvath, H. et al. (2003) Genetically engineered stem rust resistance in barley using the Rpg1 gene. Proc. Natl. Acad. Sci. U. S. A. 100, 364 – 369 151 Vol.8 No.4 April 2003 9 Takasaki, T. et al. (2000) The S receptor kinase determines selfincompatibility in Brassica stigma. Nature 403, 913 – 916 10 Braun, D.M. et al. (1997) Interaction of the maize and Arabidopsis kinase interaction domains with a subset of receptor-like protein kinases: implications for transmembrane signaling in plants. Plant J. 12, 95 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00030-X OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells Sarah M. Assmann Biology Department, Penn State University, 208 Mueller Laboratory, University Park, PA 16802-5301, USA Much of what we have learned in recent years concerning the genes that encode abscisic acid (ABA) signaling elements stems from characterization of Arabidopsis mutants with regard to a few ‘classic’ ABA responses: promotion of seed dormancy, inhibition of seed germination, regulation of root elongation, inhibition of stomatal opening and promotion of stomatal closure [1]. Of these responses, modulation of stomatal aperture is unique in being the only response that does not involve irreversible developmental changes. Rather, reversible changes in the intracellular concentrations of the osmotically active solutes Kþ, Cl2 malate22 and sucrose drive guard cell swelling or shrinking, resulting in stomatal opening or closure, respectively. Thus, one might anticipate that analysis of guard cell ABA responses might reveal some mechanisms that are largely specific to this specialized cell type. Identification of the ost1 mutant To identify such mechanisms, Anna-Chiara Mustilli, Jérôme Giraudat and colleagues [2] used an ingenious screen for guard cell effects on leaf temperature that had earlier been applied to mutants of barley by Ilya Raskin and Juanita A.R. Ladyman [3]. Given that transpirational water loss through open stomata results in leaf cooling, Jérôme Giraudat’s laboratory used remote infrared thermal imaging to screen an ethyl methane sulfonatemutagenized population for Arabidopsis mutants with cooler leaves (Fig. 1). Two allelic mutants, ost1-1 and ost1-2, as well as a third mutant, ost2, were observed to have leaf temperatures , 18C cooler than wild-type plants, while retaining a wild-type seed germination response to Corresponding author: Sarah M. Assmann ([email protected]). http://plants.trends.com ABA [4]. OST1 refers to Open STomata (stomata is Greek for mouths). Identification and characterization of the OST1 kinase Positional cloning of the OST1 gene revealed that OST1 is highly homologous to genes encoding serine –threonine protein kinases [2]. OST1 expression is limited to guard cells and vascular tissue. In a remarkable convergence of genetic and biochemical approaches, the closest relative to OST1 in the sequence databases is the ABA-activated protein kinase (AAPK) of Vicia faba, a guard-cell protein kinase initially identified by in gel kinase assays [5,6]. The AAPK cDNA was cloned based on peptide sequence obtained by de novo mass spectrometric sequence analysis [7]. OST1 is 79% identical to AAPK and, like AAPK, displays ABA-dependent autophosphorylation. ost1 mutant guard cells and V. faba guard cells expressing a dominant negative form of AAPK both exhibit an inability to engender stomatal closure in response to ABA. These and other similarities between OST1 and AAPK (Table 1) 25 Ler Leaf temperature (°C) 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. 24 23 ost1-1 22 ost1-2 21 Fig. 1. False-color infrared image of drought-stressed Ler wild type (top row), ost1-1 (middle row), and ost1-2 Arabidopsis plantlets. Temperature scale for the false color is indicated at the left of the panel. Reproduced, with permission, from Ref. [1]. 152 Update TRENDS in Plant Science Vol.8 No.4 April 2003 Table 1. Comparison of the properties of Arabidopsis thaliana OST1 and Vicia faba AAPK protein kinases Property OST1 AAPK Refs Molecular mass Expressed in guard cells but not in epidermal cells or mesophyll cells Kinase activity is dependent on prior in vivo ABA application Kinase activity is not affected by kinetin, IAA, GA3 or 2,4-D Kinase activity is Ca2þ-independent in vitro Genetic ablation results in ABA insensitivity of stomatal closure Genetic ablation results in ABA insensitivity of stomatal opening Functions downstream of abi1-1 Functions upstream of reactive oxygen species and Ca2þ Phosphorylates a single-stranded RNA-binding protein 42 kDa Yes Yes ? Yes Yes Yes Yes Yes ? 48 kDa Yes Yes Yes Yes Yes No ? ? Yes [2,5,6] [2,5] [2,5,7] [6] [2,5] [2,7] [2,7] [2] [2] [15] Abbreviations: ABA, abscisic acid; GA3, gibberellin A3; IAA, indole-3-acetic acid.; 2,4-D, 2,4-dichlorophenoxyacetic acid; ?, data not available. indicate that the two proteins are true orthologs. However, one significant difference is that the ost1 mutants are also insensitive to ABA-inhibition of stomatal opening [2], whereas V. faba stomata expressing dominant negative AAPK show normal ABA inhibition of stomatal opening [7]. Whether these differences reflect true species difference in kinase function, or differences in the experimental approaches used in the two studies (i.e. null versus dominant negative mutants or the use of different ABA concentrations) remains to be determined. OST1 also bears homology to PKABA1 of wheat, a gene whose transcript abundance in seeds increases strongly in response to ABA and dehydration [8]; however, OST1 transcript levels are not upregulated by ABA. Placing OST1 in a signaling pathway The identification of an AAPK ortholog in the genetically tractable model species Arabidopsis thaliana should enable rapid progress to be made in elucidating the AAPK/OST1 signaling pathway. A legion of signaling elements has been implicated in ABA action in guard cells, including enzymes, metabolites and ephemeral signals such as transients in cytosolic Ca2þ, pH and reactive oxygen species (ROS) (reviewed in Refs [9– 11]). By employing a dye whose fluorescence increases under oxidizing conditions, Mustilli and co-workers demonstrated that ost1-2 guard cells are deficient in ROS production in response to ABA. Application of exogenous H2O2 or Ca2þ restores stomatal closure and inhibits stomatal opening in the ost1 mutants. Because ROS are strong elicitors of plasma membrane Ca2þ channel activity [12], one could hypothesize that ost1 mutants are deficient in Ca2þ channel activation. Disruption of ABA-induced ROS production and Ca2þ channel activation in guard cells has already been demonstrated in Arabidopsis plants harboring a dominant mutation, abi1-1, in a type-2C protein phosphatase [13]. By assaying for ABA-dependent OST1 phosphorylation in the abi1-1 dominant mutant background, Mustilli et al. demonstrated that ABA stimulation of OST1 kinase activity was prevented in these mutants, suggesting that ABI1 acts upstream of OST1. Altogether, the results of the epistasis assays suggest that the signal from ABA to OST1 is modulated by ABI1 and then proceeds via ROS to regulation of cytosolic Ca2þ levels and ultimately to changes in stomatal aperture. Given that the Kþ channels that mediate Kþ uptake during stomatal opening and the http://plants.trends.com anion channels that mediate Cl2 and malate22 loss during stomatal closure are inhibited and activated by elevated cytosolic Ca2þ, respectively, it would be useful to assess to what extent altered ABA- and Ca2þ- regulation of these ion channels is responsible for the ost1 mutant phenotype. Besides protein kinases and protein phosphatases, other diverse enzymes have been implicated in the guard cell responses to ABA, including phospholipases C and D, proteins involved in RNA processing, a syntaxin, a farnesyl transferase, the small G proteins ROP10 and AtRac1, and the heterotrimeric G protein a subunit, GPA1 [9– 11,14– 18]. The relative position of OST1 in the ramifying signaling networks created by these proteins remains to be identified. Another fruitful area for future research concerns the role of other predicted protein kinases with high homology to OST1. OST1 shares 67 – 80% amino acid identity with nine other putative protein kinases of Arabidopsis, which have been given the appellation OST1-kinase-like (OSKL) 2– 10 [2]. Apparently none of these family members has redundant function with OST1 in guard cells because null mutation of ost1 suffices to confer the guard-cell ABA-insensitive phenotype. It will be interesting to ascertain whether OSKL proteins function in mediating some of the other ‘classic’ ABA responses listed at the beginning of this article or if they are involved in other, as yet unknown, functions of this vital phytohormone. Acknowledgements Supported by NSF grants MCB 9874438 and MCB 0086315. I thank members of Jérôme Giraudat’s laboratory for comments on the manuscript. References 1 Finkelstein, R.R. et al. (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15 – S45 2 Mustilli, A. et al. (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14, 3089– 3099 3 Raskin, I. and Ladyman, J.A.R. (1988) Isolation and characterization of a barley mutant with abscisic acid-insensitive stomata. Planta 173, 73 – 78 4 Merlot, S. et al. (2002) Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. Plant J. 30, 601 – 609 5 Li, J. and Assmann, S.M. (1996) An abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8, 2359– 2368 6 Mori, I.C. and Muto, S. (1997) Abscisic acid activates a 48kilodalton protein kinase in guard cell protoplasts. Plant Physiol. 113, 833 – 839 Update TRENDS in Plant Science 7 Li, J. et al. (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287, 300 – 303 8 Anderberg, R.J. and Walker-Simmons, M.K. (1992) Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proc. Natl. Acad. Sci. U. S. A. 89, 10183 – 10187 9 Hetherington, A.M. (2001) Guard cell signaling. Cell 107, 711 – 714 10 Schroeder, J.I.S. et al. (2001) Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627– 658 11 Blatt, M.R. (2000) Cellular signaling and volume control in stomatal movements of plants. Annu. Rev. Dev. Biol. 16, 221– 241 12 Pei, Z.M. et al. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406, 731 – 734 13 Murata, Y. et al. (2001) Abscisic acid activation of plasma membrane Ca2þ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen Vol.8 No.4 April 2003 14 15 16 17 18 153 species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13, 2513– 2523 Fedoroff, N.V. (2002) RNA-binding proteins in plants: the tip of an iceberg? Curr. Opin. Plant Biol. 5, 452 – 459 Li, J. et al. (2002) Modulation of an RNA-binding protein by abscisicacid-activated protein kinase. Nature 418, 793 – 797 Zheng, Z. et al. (2002) Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 14, 2787– 2797 Lemichez, E. et al. (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev. 15, 1808– 1816 Wang, X-Q. et al. (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292, 2070– 2072 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00052-9 XI International Congress on Molecular Plant–Microbe Interactions 18–27 July 2003 St Petersburg, Russia For more information, see http://www.arriam.spb.ru/mpmi/?mod=pre_an Phloem 2003 International Meeting on Phloem Transport 2003 31 August–5 September 2003 Bayreuth, Germany TOPICS: Source–sink relationships in nutrient allocation; phloem development and differentiation; phloem as a pathway for signal substances; phloem interactions with pathogens and herbivores. For more information contact: Professor Ewald Komor, Plant Physiology, University Bayreuth, D-95440 Bayreuth, Germany e-mail: [email protected] http://www.phloem2003.de/ http://plants.trends.com