Abstract
In the past few years, molecular cloning studies have revealed the primary structure of plant protein serine/threonine phosphatases. Two structurally distinct families, the PP1/PP2A family and the PP2C family, are present in plants as well as in animals. This review will focus on the plant PP2C family of protein phosphatases. Biochemical and molecular genetic studies in Arabidopsis have identified PP2C enzymes as key players in plant signal transduction processes. For instance, the ABI1/ABI2 PP2Cs are central components in abscisic acid (ABA) signal transduction. Arabidopsis mutants containing a single amino acid exchange in ABI1 or ABI2 show a reduced response to ABA. Another member of the PP2C family, kinase-associated protein phosphatase (KAPP), appears to be an important element in some receptor-like kinase (RLK) signalling pathways. Finally, an alfalfa PP2C acts as a negative regulator of a plant mitogen-activated protein kinase (MAPK) pathway. Thus, the plant PP2Cs function as regulators of various signal transduction pathways.
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Becraft PW, Stinard PS, McCarty DR: CRINKL Y4: a TNFR like receptor kinase involved in maize epidermal differentiation. Science 273: 1406–1409 (1996).
Bertauche N, Leung J, Giraudat J: Protein phosphatase activity of abscisic acid insensitive1 (ABI1) protein from Arabidopsis thaliana. Eur J Biochem 241: 193–200 (1996).
Bleecker AB, Schaller GE: The mechanism of ethylene perception. Plant Physiol 111: 653–660 (1996).
Bork P, Brown NP, Hegyi H, Schultz J: The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci 5: 1421–1425 (1996).
Bögre L, Ligterink W, Meskiene I, Barker PJ, Heberle-Bors E, Huskisson NS, Hirt H: Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 9: 75–83 (1997).
Braun DM, Stone JM, Walker JC: 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: 83–95 (1997).
Bruxelles GL: Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiol 111: 381–391 (1996).
Chandler PM, Robertson M: Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45: 113–141 (1994).
Chang C, Schaller GE, Patterson SE, Kwok SF, Meyerowitz EM, Bleecker AB: The TMK1 gene from Arabidopsis codes for a protein with structural and biochemical characteristics of a receptor protein kinase. Plant Cell 4: 1263–1271 (1992).
Chen MX, McPartlin AE, Brown L, Chen YH, Barker HM, Cohen PTW: A novel human protein serine/threonine phosphatase, which possesses four tetratricopeptide repeat motifs and localizes to the nucleus. EMBO J 13: 4278–4290 (1994).
Clark SE, Willians RW, Meyerowitz EM: The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Aribidopsis. Cell 89: 575–585 (1997).
Cohen P, Cohen PTW: Protein phosphatases come of age. J Biol Chem 264: 21435–21438 (1989).
Cohen P: The structure and regulation of protein phosphatases. Annu Rev Biochem 58: 453–508 (1989).
Cohen PTW: Nomenclature and chromosomal localization of human protein serine/threonine phosphatase genes. Adv Prot Phos 8: 371–374 (1994).
Corton JM, Gillespie JG, Hardie DG: Role of the AMPactivated protein kinase in the cellular stress response. Curr Biol 4: 315–324 (1994).
Das AK, Helps NR, Cohen PTW, Barford D: Crystal structure of protein serine/threonine phosphatase 2C at 2.0 Å resolution. EMBO J 15: 6798–6809 (1996).
Duncan L, Alper S, Arigoni F, Losick R, Stragier P: Activation of cell-specific transcription by a serine phosphatase at the site of asymmetric division. Science 270: 641–644 (1995).
Fantl WJ, Johnson DE, Williams LT: Signaling by receptor tyrosine kinases. Annu Rev Biochem 62: 453–481 (1993).
Finkelstein RR, Somerville CR: Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol 94: 1172–1179 (1990).
Gaits F, Shiozaki K, Russel P: Protein phosphatase 2C acts independently of stress-activated kinase cascade to regulate the stress response in fission yeast. J Biol Chem 272: 17873–17879 (1997).
Gilmour SJ, Thomashow MF: Cold acclimation and coldregulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17: 1233–1240 (1991).
Gosti F, Bertauche N, Vartanian N, Giraudat J: Abscisic aciddependent and-independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246: 10–18 (1995).
Herbst R, Carroll PM, Allard JD, Schilling J, Raabe T, Simon MA: Daughter of Sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during Sevenless signaling. Cell 85: 899–909 (1996).
Herskowitz I: Functional inactivation of genes by dominant negative mutations. Nature 329: 219–222 (1987).
Hubbard MJ, Cohen P: On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci 18: 172–177 (1993).
Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H: Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93: 11274–11279 (1996).
Klee CB, Draetta GF, Hubbard MJ: Calcineurin. Adv Enzymol 61: 149–200 (1988).
Koornneef M, Reuling G, Karssen CM: The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61: 377–383 (1984).
Kuromori T, Yamamoto M: Cloning of cDNAs from Arabidopsis thaliana that encode a putative protein phosphatase 2C and a human Dr1-like protein by transformation of a fission yeast mutant. Nucl Acids Res 22: 5296–5301 (1994).
Leube MP, Grill E, Amrhein N: ABI1 of Arabidopsis is a protein serine/threonine phosphatase highly regulated by proton and magnesium ion concentration. FEBS Lett 424: 96–100 (1998).
Leung J, Bouvier-Durand M, Morris P-C, Guerrier D, Chefdor F, Giraudat J: Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448–1452 (1994).
Leung J, Merlot S, Giraudat J: The Arabidopsis abscisic acid-insensitive2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759–771 (1997).
Li J, Chory J: A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938 (1997).
Luan S, Li W, Rusnak F, Assmann SM, Schreiber SL: Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. Proc Natl Acad Sci USA 90: 2202–2206 (1993).
Maeda T, Wurgler-Murphy SM, Saito H: A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242–245 (1994).
Mayer-Jaekel RE, Hemmings BA: Protein phosphatase 2A: a ‘ménage à trios’. Trends Cell Biol 4: 287–291 (1994).
McGowan CH, Cohen P: Protein phosphatase 2C from rabbit skeletal muscle and liver: an Mg2+ dependent enzyme. Meth Enzymol 159: 416–426 (1988).
McGrath JM, Jancso MM, Pichersky E: Duplicate sequences with a similarity to expressed genes in the genome of Arabidopsis thaliana. Theor Appl Genet 86: 880–888 (1993).
Merlot S, Giraudat J: Genetic analysis of abscisic acid signal transduction. Plant Physiol 114: 751–757 (1997).
Meskiene I, Bögre L, Glaser W, Balog J, Brandstötter M, Zwerger K, Ammerer G, Hirt H: MP2C, a plant protein phosphatase 2C, functions as a negative regulator of mitogenactivated protein kinase pathways in yeast and plants. Proc Natl Acad Sci USA 95: 1938–1943 (1998).
Meyer K, Leube MP, Grill E: A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452–1455 (1994).
Milarski KL, Saltiel AR: Expression of catalytically inactive Syp phosphatase in 3T3 cells blocks stimulation of mitogenactivated protein kinase by insulin. J Biol Chem 269: 21239–21243 (1994).
Moncrief ND, Kretsinger RH, Goodman M: Evolution of EFhand calcium-modulated proteins. I. Relationships based on amino acid sequences. J Mol Evol 30: 522–562 (1990).
Moore F, Weekes J, Hardie DG: Evidence that AMP triggers phosphorylation as well as direct allosteric activation of rat liver AMP-activated protein kinase. Eur J Biochem 199: 691–697 (1991).
Pei Z-M, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI: Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9: 409–423 (1997).
Pickett FB, Meeks-Wagner DR: Seeing double: appreciating genetic redundancy. Plant Cell 7: 1347–1356 (1995).
Rodriguez PL, Benning G, Grill E: ABI2, a second protein phosphatase 2C involved in ABA signal transduction in Arabidopsis. FEBS Lett 421: 185–190 (1998).
Rodriguez PL, Leube M, Grill E: Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2. Plant Mol Biol (1988), in press.
Schreiber SL: Immunophilin-sensitive phosphatase action in cell signaling pathways. Cell 70: 365–368 (1992).
Sheen J: Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274: 1900–1902 (1996).
Sheen J: Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc Natl Acad Sci USA 95: 975–980 (1998).
Shenolikar S: Protein serine/threonine phosphatases: new avenues for cell regulation. Annu Rev Cell Biol 10: 55–86 (1994).
Shibasaki F, Price ER, Milan D, Mckeon F: Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382: 370–373 (1996).
Shiozaki K, Russell P: Counteractive roles of protein phosphatase 2C (PP2C) and a MAP kinase kinase homolog in the osmoregulation of fission yeast. EMBO J 14: 492–502 (1995).
Smith RD, Walker JC: Plant protein phosphatases. Annu Rev Plant Physiol Plant Mol Biol 47: 101–125 (1996).
Song W-Y, Wang G-L-, Chen L-L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhao W-X, Zhu L-H, Fauquet C, Ronald P: A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804–1806 (1995).
Söderman E, Mattsson J, Engström P: The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10: 375–381 (1996).
Stark MJR: Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation. Yeast 12: 1647–1675 (1996).
Stone JM, Collinge MA, Smith RD, Horn MA, Walker JC: Interaction of a protein phosphatase with an Arabidopsis serinethreonine receptor kinase. Science 266: 793–795 (1994).
Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L: Differential expression of two P5CS genes controlling proline accumulation during saltstress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12: 557–569 (1997).
Sun H, Charles CH, Lau LF, Tonks NK: MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75: 487–493 (1993).
Tamura S, Lynch KR, Larner J, Fox J, Yasui A, Kikuchi K, Suzuki Y, Tsuiki S: Molecular cloning of rat type 2C (IA) protein phosphatase mRNA. Proc Natl Acad Sci USA 86: 1796–1800 (1989).
Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y: The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746 (1996).
Ullrich A, Sclessinger J: Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212 (1990).
Vartanian N, Marcotte L, Giraudat J: Drought rhizogenesis in Arabidopsis thaliana. Plant Physiol 104: 761–767 (1994).
Walker JC: Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3: 451–456 (1993).
Walker JC: Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26: 1599–1609 (1994).
Williams RW, Wilson JM, Meyerowitz EM: A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci USA 94: 10467–10472 (1997).
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Rodriguez, P.L. Protein phosphatase 2C (PP2C) function in higher plants. Plant Mol Biol 38, 919–927 (1998). https://doi.org/10.1023/A:1006054607850
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DOI: https://doi.org/10.1023/A:1006054607850