Artículo

Chinchilla, D.; Frugier, F.; Raices, M.; Merchan, F.; Giammaria, V.; Gargantini, P.; Gonzalez-Rizzo, S.; Crespi, M.; Ulloa, R. "A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots" (2008) Functional Plant Biology. 35(1):92-101
La versión final de este artículo es de uso interno de la institución.
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

A family of plant kinases containing ankyrin-repeats, the Ankyrin-Protein Kinases (APKs), shows structural resemblance to mammalian Integrin-Linked Kinases (ILKs), key regulators of mammalian cell adhesion. MsAPK1 expression is induced by osmotic stress in roots of Medicago sativa (L.) plants. The Escherichia coli-purified MsAPK1 could only phosphorylate tubulin among a variety of substrates and the enzymatic activity was strictly dependent on Mn2+. MsAPK1 is highly related to two APK genes in Arabidopsis thaliana (L.), AtAPK1 and AtAPK2. Promoter-GUS fusions assays revealed that the Arabidopsis APK genes show distinct expression patterns in roots and hypocotyls. Although Medicago truncatula (L.) plants affected in MsAPK1 expression could not be obtained using in vitro regeneration, A. thaliana plants expressing MsAPK1 or a mutant MsAPK1 protein, in which the conserved aspartate 315 of the kinase catalytic domain was replaced by asparagines (DN-lines), developed normally. The DN mutant lines showed increased capacity to develop adventitious roots when compared with control or MsAPK1-expressing plants. APK-mediated signalling may therefore link perception of external abiotic signals and the microtubule cytoskeleton, and influence adventitious root development. © CSIRO 2008.

Registro:

Documento: Artículo
Título:A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots
Autor:Chinchilla, D.; Frugier, F.; Raices, M.; Merchan, F.; Giammaria, V.; Gargantini, P.; Gonzalez-Rizzo, S.; Crespi, M.; Ulloa, R.
Filiación:Institut des Sciences du Végétal (ISV), CNRS, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, France
Instituto de Investigaciones en Ingeniería Genética Y Biología Molecular, INGEBI, FCEN-UBA, Vuelta de Obligado 2490, Buenos Aires, 1428, Argentina
Botanical Institute, University of Basel, Hebelstrasse 1, CH-4056, Basel, Switzerland
Salk Institute for Biological Studies, San Diego, CA 92037, United States
Palabras clave:Arabidopsis thaliana; Tubulin phosphorylation; Cell adhesion; Escherichia coli; Gene expression; Osmosis; Phosphorylation; Plants (botany); Arabidopsis thaliana; Microtubule cytoskeleton; Osmotic stress; Tubulin phosphorylation; Enzymes; alfalfa; angiosperm; catalysis; enzyme activity; gene expression; phosphorus; protein; root; Arabidopsis; Arabidopsis thaliana; Escherichia coli; Mammalia; Medicago sativa; Medicago truncatula
Año:2008
Volumen:35
Número:1
Página de inicio:92
Página de fin:101
DOI: http://dx.doi.org/10.1071/FP07209
Título revista:Functional Plant Biology
Título revista abreviado:Funct. Plant Biol.
ISSN:14454408
CODEN:FPBUC
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_14454408_v35_n1_p92_Chinchilla

Referencias:

  • Aletta JM (1996) Phosphorylation of type III beta-tubulin PC12 cell neurites during NGF-induced process outgrowth. Journal of Neurobiology 31, 461-475. doi: 10.1002/(SICI)1097-4695(199612)31:4〈461:: AIDNEU6〉3.0.CO;2-7; Aloni, R., Aloni, E., Langhans, M., Ullrich, C.I., Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism (2006) Annals of Botany, 97, pp. 883-893. , doi: 10.1093/aob/mcl027
  • Alvarez, R., Nissen, S.J., Sutter, E.G., Relationship between indole-3-acetic acid levels in apple (Malus pumila Mill.) rootstocks cultured in vitro and adventitious root formation in the presence of indole-3-butyric acid (1989) Plant Physiology, 89, pp. 439-443
  • Barizza, E., Lo Schiavo, F., Terzi, M., Filippini, F., Evidence suggesting protein tyrosine phosphorylation in plants depends on the developmental conditions (1999) FEBS Letters, 447, pp. 191-194. , doi: 10.1016/S0014-5793(99) 00272-0
  • Baskin, T.I., Wilson, J.E., Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules (1997) Plant Physiology, 113, pp. 493-502. , doi: 10.1104/pp.113.2.493
  • Bechtold, N., Pelletier, G., In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration (1998) Methods in Molecular Biology (Clifton, N.J.), 82, pp. 259-266
  • Blazkova, A., Sotta, B., Tranvan, H., Maldiney, R., Bonnet, M., Einhorn, J.H., Kerhoas, L., Miginiac, E., Auxin metabolism and rooting in young and mature clones of Sequoia sempervivens (1997) Physiologia Plantarum, 99, pp. 73-80. , doi: 10.1111/j.1399-3054.1997.tb03433.x
  • Boerjan, W., Cervera, M.T., Delarue, M., Beeckman, T., Dewitte, W., Bellini, C., Caboche, M., Inze, D., Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction (1995) The Plant Cell, 7, pp. 1405-1419. , doi: 10.2307/3870131
  • Bogre, L., Calderini, O., Binarova, P., Mattauch, M., Till, S., A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division (1999) The Plant Cell, 11, pp. 101-113. , doi: 10.2307/3870841
  • Boudeau, J., Miranda-Saavedra, D., Barton, G.J., Alessi, D.R., Emerging roles of pseudokinases (2006) Trends in Cell Biology, 16, pp. 443-452. , doi: 10.1016/j.tcb.2006.07.003
  • Camilleri, C., Azimzadeh, J., Pastuglia, M., Bellini, C., Grandjean, O., Bouchez, D., The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton (2002) The Plant Cell, 14, pp. 833-845. , doi: 10.1105/tpc.010402
  • Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P., Sandberg, G., Bennett, M.J., Dissecting Arabidopsis lateral root development (2003) Trends in Plant Science, 8, pp. 165-171. , doi: 10.1016/S1360-1385(03) 00051-7
  • Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Auxin transport promotes Arabidopsis lateral root initiation (2001) The Plant Cell, 13, pp. 843-852. , doi: 10.2307/3871344
  • Celenza, J.L., Grifasi, P.L., Fink, G.R., A pathway for lateral root formation in Arabidopsis thaliana (1995) Genes & Development, 9, pp. 2131-2142. , doi: 10.1101/gad.9.17.2131
  • Chinchilla, D., Merchan, F., Megias, M., Kondorosi, A., Sousa, C., Crespi, M., Ankyrin protein kinases, a novel type of plant kinase gene whose expression is induced by osmotic stress in alfalfa (2003) Plant Molecular Biology, 51, pp. 555-566. , doi: 10.1023/A:1022337221225
  • Crespi, M., Galvez, S., Molecular mechanisms in root nodule development (2000) Journal of Plant Growth Regulation, 19, pp. 155-166
  • Crespi, M., Jurkevitch, E., Poiret, M., D'Aubenton-Carafa, Y., Petrovics, G., Kondorosi, E., Kondorosi, A., enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth (1994) The EMBO Journal, 13, pp. 5099-5112
  • Delarue, M., Prinsen, E., Onckelen, H.V., Caboche, M., Bellini, C., sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis (1998) The Plant Journal, 14, pp. 603-611. , doi: 10.1046/j.1365-313X.1998.00163.x
  • Delcommenne, M., Tan, C., Gray, V., Rue, L., Woodgett, J., Dedhar, S., Phosphoinositide-3-OH kinase dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase (1998) Proceedings of the National Academy of Sciences of the United States of America, 95, pp. 11211-11216. , doi: 10.1073/pnas.95.19.11211
  • Deruère, J., Jackson, K., Garbers, C., Söll, D., DeLong, A., The RCN1-encoded A subunit of protein phosphatase 2A increases phosphatase activity in vivo (1999) The Plant Journal, 20, pp. 389-399. , doi: 10.1046/j.1365-313x.1999.00607.x
  • Epstein, E., Ludwig-Müller, J., Indole-3-butyric acid in plants: Occurrence, biosynthesis, metabolism, and transport (1993) Physiologia Plantarum, 88, pp. 382-389. , doi: 10.1111/j.1399-3054.1993.tb05513.x
  • Feng, Y., Hodge, D.R., Palmieri, G., Chase, D.L., Longo, D.L., Ferris, D.K., Association of polo-like kinase with alpha-, beta- and gamma-tubulins in a stable complex (1999) The Biochemical Journal, 339, pp. 435-442. , doi: 10.1042/0264-6021:3390435
  • Fowler, J.E., Quatrano, R.S., Plant cell morphogenesis: Plasma membrane interactions with the cytoskeleton and cell wall (1997) Annual Review of Cell and Developmental Biology, 13, pp. 697-743. , doi: 10.1146/annurev.cellbio.13.1. 697
  • Frugier, F., Poirier, S., Satiat-Jeunemaître, B., Kondorosi, A., Crespi, M., A Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis (2000) Genes & Development, 14, pp. 475-482
  • Gargantini, P.R., Gonzalez-Rizzo, S., Chinchilla, D., Raices, M., Giammaria, V., Ulloa, R.M., Frugier, F., Crespi, M.D., A CDPK isoform participates in the regulation of nodule number in Medicago truncatula (2006) The Plant Journal, 48, pp. 843-856. , doi: 10.1111/j.1365-313X.2006.02910.x
  • Hemerly, A., Engler, J.A., Bergounioux, C., Van Montagu, M., Engler, G., Inze, D., Ferreira, P., Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development (1995) The EMBO Journal, 14, pp. 3925-3936
  • Hemsley, R., McCutcheon, S., Doonan, J., Lloyd, C., P34 (cdc2) kinase is associated with cortical microtubules from higher plant protoplasts (2001) FEBS Letters, 508, pp. 157-161. , doi: 10.1016/S0014-5793(01)03046-0
  • Huang, H.J., Lin, Y.M., Huang, D.D., Takahashi, T., Sugiyama, M., Protein tyrosine phosphorylation during phytohormone-stimulated cell proliferation in Arabidopsis hypocotyls (2003) Plant & Cell Physiology, 44, pp. 770-775. , doi: 10.1093/pcp/pcg082
  • Flores II, I., Oropeza, C., Hernandez-Sotomayor, S.M., Protein phosphorylation during coconut zygotic embryo development (1998) Plant Physiology, 118, pp. 257-263. , doi: 10.1104/pp.118.1.257
  • Jefferson, R.A., Kavanagh, T.A., Bevan, M.W., GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants (1987) The EMBO Journal, 6, pp. 3901-3907
  • Kameyama, K., Kishi, Y., Yoshimura, M., Kanzawa, N., Sameshima, M., Tsuchiya, T., Tyrosine phosphorylation in plant bending (2000) Nature, 407, p. 37. , doi: 10.1038/35024149
  • King, J.J., Stimart, D.P., Fisher, R.H., Bleecker, A.B., A mutation altering auxin homeostasis and plant morphology in Arabidopsis (1995) The Plant Cell, 7, pp. 2023-2037. , doi: 10.2307/3870148
  • Kohorn, B.D., Kobayashi, M., Johansen, S., Riese, J., Huang, L.F., Koch, K., Fu, S., Byers, N., An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth (2006) The Plant Journal, 46, pp. 307-316. , doi: 10.1111/j.1365-313X.2006.02695.x
  • Komis, G., Apostolakos, P., Gaitanaki, C., Galatis, B., Hyperosmotically induced accumulation of a phosphorylated p38-like MAPK involved in protoplast volume regulation of plasmolyzed wheat root cells (2004) FEBS Letters, 573, pp. 168-174. , doi: 10.1016/j.febslet.2004.07.065
  • Konishi, M., Sugiyama, M., Genetic analysis of adventitious root formation with a novel series of temperature-sensitive mutants of Arabidopsis thaliana (2003) Development, 130, pp. 5637-5647. , doi: 10.1242/dev.00794
  • Koontz, D.A., Choi, J.H., Protein phosphorylation in carrot somatic embryos in response to abscisic acid (1993) Plant Physiology and Biochemistry, 31, pp. 95-102
  • Lopez-Bucio, J., Cruz-Ramirez, A., Herrera-Estrella, L., The role of nutrient availability in regulating root architecture (2003) Current Opinion in Plant Biology, 6, pp. 280-287. , doi: 10.1016/S1369-5266(03)00035-9
  • Ludwig-Muller, J., Vertocnik, A., Town, C.D., Analysis of indole-3-butyric acid induced adventitious root formation on Arabidopsis stem segments (2005) Journal of Experimental Botany, 56, pp. 2095-2105. , doi: 10.1093/jxb/eri208
  • MacRae, T.H., Tubulin post-translational modification-enzymes and their mechanisms of action (1997) European Journal of Biochemistry, 244, pp. 265-278. , doi: 10.1111/j.1432-1033.1997.00265.x
  • Malamy, J.N., Benfey, P.N., Organization and cell differentiation in lateral roots of Arabidopsis thaliana (1997) Development, 124, pp. 33-44
  • Malamy, J.E., Ryan, K.S., Environmental regulation of lateral root initiation in Arabidopsis (2001) Plant Physiology, 127, pp. 899-909. , doi: 10.1104/pp.127.3.899
  • Naska, S., Park, K.J., Hannigan, G.E., Dedhar, S., Miller, F.D., Kaplan, D.R., An essential role for the integrin-linked kinase-glycogen synthase kinase-3 beta pathway during dendrite initiation and growth (2006) Journal of Neuroscience, 26, pp. 13344-13356. , doi: 10.1523/JNEUROSCI.4462-06.2006
  • Nishihama, R., Soyano, T., Ishikawa, M., Araki, S., Tanaka, H., Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex (2002) Cell, 109, pp. 87-99. , doi: 10.1016/S0092- 8674(02)00691-8
  • Qian, Y., Zhong, X., Flynn, D.C., Zheng, J.Z., Qiao, M., Wu, C., Dedhar, S., Jiang, B.H., ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling (2005) Oncogene, 24, pp. 3154-3165. , doi: 10.1038/sj.onc.1208525
  • Raices, M., Gargantini, P.R., Chinchilla, D., Crespi, M., Tellez-Inon, M.T., Ulloa, R.M., Regulation of CDPK isoforms during tuber development (2003) Plant Molecular Biology, 52, pp. 1011-1024. , doi: 10.1023/A:1025478315648
  • Reddy, M.M., Rajasekharan, R., Role of threonine residues in the regulation of manganese-dependent arabidopsis serine/threonine/tyrosine protein kinase activity (2006) Archives of Biochemistry and Biophysics, 455, pp. 99-109. , doi: 10.1016/j.abb.2006.09.009
  • Reed, R.C., Brady, S.R., Muday, G.K., Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis (1998) Plant Physiology, 118, pp. 1369-1378. , doi: 10.1104/pp.118.4.1369
  • Rodríguez-Zapata, L.C., Hernández-Sotomayor, S.M., Evidence of protein-tyrosine kinase activity in Catharanthus roseus roots transformed by Agrobacterium rhizogenes (1997) Planta, 204, pp. 70-77. , doi: 10.1007/s004250050231
  • Rudrabhatla, P., Reddy, M.M., Rajasekharan, R., Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases (2006) Plant Molecular Biology, 60, pp. 293-319. , doi: 10.1007/s11103-005-4109- 7
  • Sakurai, M., Pak, J.Y., Muramatsu, Y., Fukuhara, T., Integrin-like protein at the invaginated plasma membrane of epidermal cells in mature leaves of the marine angiosperm Zostera marina L (2004) Planta, 220, pp. 271-277. , doi: 10.1007/s00425-004-1348-9
  • Sedgwick, S.G., Smerdon, S.J., The ankyrin repeat: A diversity of interactions on a common structural framework (1999) Trends in Biochemical Sciences, 24, pp. 311-316. , doi: 10.1016/S0968-0004(99)01426-7
  • Smith, R.D., Walker, J.C., Plant protein phosphatases (1996) Annual Review of Plant Physiology and Plant Molecular Biology, 47, pp. 101-125. , doi: 10.1146/annurev.arplant.47.1.101
  • Szabados, L., Charrier, B., Kondorosi, A., de Bruijn, F.J., Ratet, P., New plant promoter and enhancer testing vectors (1995) Molecular Breeding, 1, pp. 419-423. , doi: 10.1007/BF01248419
  • Tabe, Y., Jin, L., Satsuma-Ishii, Y., Xu, Y., McQueen, T., Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells (2007) Cancer Research, 67, pp. 684-694. , doi: 10.1158/0008-5472.CAN-06-3166
  • Tavares, A.A., Glover, D.M., Sunkel, C.E., The conserved mitotic kinase polo is regulated by phosphorylation and has preferred microtubule-associated substrates in Drosophila embryo extracts (1996) The EMBO Journal, 15, pp. 4873-4883
  • Taylor, S.S., Knighton, D.R., Zheng, J., Sowadski, J.M., Gibbs, C.S., Zoller, M.J., A template for the protein kinase family (1993) Trends in Biochemical Sciences, 18, pp. 84-89. , doi: 10.1016/0968-0004(93)80001-R
  • Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., Murakami, Y., Madsen, L.H., Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development (2006) Nature, 441, pp. 1153-1156. , doi: 10.1038/nature04862
  • Tripp, K.W., Barrick, D., Enhancing the stability and folding rate of a repeat protein through the addition of consensus repeats (2007) Journal of Molecular Biology, 365, pp. 1187-1200. , doi: 10.1016/j.jmb.2006.09.092
  • Ullah, H., Chen, J.G., Temple, B., Boyes, D.C., Alonso, J.M., Davis, K.R., Ecker, J.R., Jones, A.M., The beta-subunit of the Arabidopsis G protein negatively regulates auxin induced cell division and affects multiple developmental processes (2003) The Plant Cell, 15, pp. 393-409. , doi: 10.1105/tpc.006148
  • Ulloa, R.M., Torres, H.N., Ochatt, C.M., Téllez-Iñón, M.T., Ca2+-Calmodulin dependent protein kinase activity in the ascomycetes Neurospora crassa (1991) Molecular and Cellular Biochemistry, 10, pp. 155-163
  • Vogel, J., Drapkin, B., Oomen, J., Beach, D., Bloom, K., Snyder, M., Phosphorylation of gamma-tubulin regulates microtubule organization in budding yeast (2001) Developmental Cell, 1, pp. 621-631. , doi: 10.1016/S1534-5807(01) 00073-9
  • Whittington, A.T., Vugrek, O., Wei, K.J., Hasenbein, N.G., Sugimoto, K., Rashbrooke, M.C., Wasteneys, G.O., MOR1 is essential for organizing cortical microtubules in plants (2001) Nature, 411, pp. 610-613. , doi: 10.1038/35079128
  • Wu, C., Dedhar, S., Integrin-linked kinase (ILK) and its interactors: A new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes (2001) Journal of Cell Biology, 155, pp. 505-510. , doi: 10.1083/jcb.200108077
  • Yang, T., Du, L., Poovaiah, B.W., Concept of redesigning proteins by manipulating calcium/calmodulin binding domains to engineer plants with altered traits (2007) Functional Plant Biology, 34, pp. 343-352. , doi: 10.1071/FP06293
  • Zhang, H., Forde, B.G., Regulation of Arabidopsis root development by nitrate availability (2000) Journal of Experimental Botany, 51, pp. 51-59. , doi: 10.1093/jexbot/51.342.51

Citas:

---------- APA ----------
Chinchilla, D., Frugier, F., Raices, M., Merchan, F., Giammaria, V., Gargantini, P., Gonzalez-Rizzo, S.,..., Ulloa, R. (2008) . A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots. Functional Plant Biology, 35(1), 92-101.
http://dx.doi.org/10.1071/FP07209
---------- CHICAGO ----------
Chinchilla, D., Frugier, F., Raices, M., Merchan, F., Giammaria, V., Gargantini, P., et al. "A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots" . Functional Plant Biology 35, no. 1 (2008) : 92-101.
http://dx.doi.org/10.1071/FP07209
---------- MLA ----------
Chinchilla, D., Frugier, F., Raices, M., Merchan, F., Giammaria, V., Gargantini, P., et al. "A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots" . Functional Plant Biology, vol. 35, no. 1, 2008, pp. 92-101.
http://dx.doi.org/10.1071/FP07209
---------- VANCOUVER ----------
Chinchilla, D., Frugier, F., Raices, M., Merchan, F., Giammaria, V., Gargantini, P., et al. A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots. Funct. Plant Biol. 2008;35(1):92-101.
http://dx.doi.org/10.1071/FP07209