A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots
Delphine Chinchilla A C , Florian Frugier A , Marcela Raices B D , Francisco Merchan A , Veronica Giammaria B , Pablo Gargantini B , Silvina Gonzalez-Rizzo A , Martin Crespi A E and Rita Ulloa B EA Institut des Sciences du Végétal (ISV), CNRS, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.
B Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, INGEBI, FCEN-UBA, Vuelta de Obligado 2490, 2do piso, Buenos Aires, 1428 Argentina.
C Present address: Botanical Institute, University of Basel, Hebelstrasse 1, CH-4056, Basel, Switzerland.
D Present address: The Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
E Corresponding authors. Emails: martin.crespi@isv.cnrs-gif.fr; rulloa@dna.uba.ar
Functional Plant Biology 35(1) 92-101 https://doi.org/10.1071/FP07209
Submitted: 31 August 2007 Accepted: 14 December 2007 Published: 25 January 2008
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.
Additional keywords: Arabidopsis thaliana, tubulin phosphorylation.
Acknowledgements
We thank the Platform of Cell Biology and Spencer Brown for helping in confocal microscopy analysis. Screening of the AtAPK1 mutant was performed in the laboratory of David Bouchez (INRA Versailles, France) with the help of Fabienne Granier. Simone Poirier was involved in the generation of Medicago truncatula transgenics. Finally, we thank Rafael Pont-Lezica and Yves Henry for helpful suggestions and discussions. D.C. was recipient of a fellowship from the Ministère de l’Enseignement Supérieur et de la Recherche. M.R., P.G. and V.G. were fellows of CONICET. This work was partially done in the frame of the Ecos-Sud Program (CNRS/France-SeCyT/Argentina).
Aletta JM
(1996) Phosphorylation of type III beta-tubulin PC12 cell neurites during NGF-induced process outgrowth. Journal of Neurobiology 31, 461–475.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Aloni R,
Aloni E,
Langhans M, Ullrich CI
(2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97, 883–893.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alvarez R,
Nissen SJ, Sutter EG
(1989) 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. Plant Physiology 89, 439–443.
| PubMed |
Barizza E,
Lo Schiavo F,
Terzi M, Filippini F
(1999) Evidence suggesting protein tyrosine phosphorylation in plants depends on the developmental conditions. FEBS Letters 447, 191–194.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Baskin TI, Wilson JE
(1997) Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules. Plant Physiology 113, 493–502.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bechtold N, Pelletier G
(1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods in Molecular Biology (Clifton, N.J.) 82, 259–266.
| PubMed |
Blazkova A,
Sotta B,
Tranvan H,
Maldiney R,
Bonnet M,
Einhorn JH,
Kerhoas L, Miginiac E
(1997) Auxin metabolism and rooting in young and mature clones of Sequoia sempervivens. Physiologia Plantarum 99, 73–80.
| Crossref | GoogleScholarGoogle Scholar |
Boerjan W,
Cervera MT,
Delarue M,
Beeckman T,
Dewitte W,
Bellini C,
Caboche M,
Van Onckelen H,
Van Montagu M, Inze D
(1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. The Plant Cell 7, 1405–1419.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bogre L,
Calderini O,
Binarova P,
Mattauch M, Till S , et al.
(1999) A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. The Plant Cell 11, 101–113.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boudeau J,
Miranda-Saavedra D,
Barton GJ, Alessi DR
(2006) Emerging roles of pseudokinases. Trends in Cell Biology 16, 443–452.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Camilleri C,
Azimzadeh J,
Pastuglia M,
Bellini C,
Grandjean O, Bouchez D
(2002) The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. The Plant Cell 14, 833–845.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Casimiro I,
Beeckman T,
Graham N,
Bhalerao R,
Zhang H,
Casero P,
Sandberg G, Bennett MJ
(2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Casimiro I,
Marchant A,
Bhalerao RP,
Beeckman T, Dhooge S , et al.
(2001) Auxin transport promotes Arabidopsis lateral root initiation. The Plant Cell 13, 843–852.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Celenza JL,
Grifasi PL, Fink GR
(1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes & Development 9, 2131–2142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chinchilla D,
Merchan F,
Megias M,
Kondorosi A,
Sousa C, Crespi M
(2003) Ankyrin protein kinases, a novel type of plant kinase gene whose expression is induced by osmotic stress in alfalfa. Plant Molecular Biology 51, 555–566.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Crespi M, Galvez S
(2000) Molecular mechanisms in root nodule development. Journal of Plant Growth Regulation 19, 155–166.
| PubMed |
Crespi M,
Jurkevitch E,
Poiret M,
D’Aubenton-Carafa Y,
Petrovics G,
Kondorosi E, Kondorosi A
(1994) enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. The EMBO Journal 13, 5099–5112.
| PubMed |
Delarue M,
Prinsen E,
Onckelen HV,
Caboche M, Bellini C
(1998) sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. The Plant Journal 14, 603–611.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delcommenne M,
Tan C,
Gray V,
Rue L,
Woodgett J, Dedhar S
(1998) Phosphoinositide-3-OH kinase dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proceedings of the National Academy of Sciences of the United States of America 95, 11211–11216.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Deruère J,
Jackson K,
Garbers C,
Söll D, DeLong A
(1999) The RCN1-encoded A subunit of protein phosphatase 2A increases phosphatase activity in vivo. The Plant Journal 20, 389–399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Epstein E, Ludwig-Müller J
(1993) Indole-3-butyric acid in plants: occurrence, biosynthesis, metabolism, and transport. Physiologia Plantarum 88, 382–389.
| Crossref | GoogleScholarGoogle Scholar |
Feng Y,
Hodge DR,
Palmieri G,
Chase DL,
Longo DL, Ferris DK
(1999) Association of polo-like kinase with alpha-, beta- and gamma-tubulins in a stable complex. The Biochemical Journal 339, 435–442.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fowler JE, Quatrano RS
(1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annual Review of Cell and Developmental Biology 13, 697–743.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Frugier F,
Poirier S,
Satiat-Jeunemaître B,
Kondorosi A, Crespi M
(2000) A Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis. Genes & Development 14, 475–482.
| PubMed |
Gargantini PR,
Gonzalez-Rizzo S,
Chinchilla D,
Raices M,
Giammaria V,
Ulloa RM,
Frugier F, Crespi MD
(2006) A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. The Plant Journal 48, 843–856.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hemerly A,
Engler JA,
Bergounioux C,
Van Montagu M,
Engler G,
Inze D, Ferreira P
(1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. The EMBO Journal 14, 3925–3936.
| PubMed |
Hemsley R,
McCutcheon S,
Doonan J, Lloyd C
(2001) P34 (cdc2) kinase is associated with cortical microtubules from higher plant protoplasts. FEBS Letters 508, 157–161.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huang HJ,
Lin YM,
Huang DD,
Takahashi T, Sugiyama M
(2003) Protein tyrosine phosphorylation during phytohormone-stimulated cell proliferation in Arabidopsis hypocotyls. Plant & Cell Physiology 44, 770–775.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Islas-Flores II,
Oropeza C, Hernandez-Sotomayor SM
(1998) Protein phosphorylation during coconut zygotic embryo development. Plant Physiology 118, 257–263.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jefferson RA,
Kavanagh TA, Bevan MW
(1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6, 3901–3907.
| PubMed |
Kameyama K,
Kishi Y,
Yoshimura M,
Kanzawa N,
Sameshima M, Tsuchiya T
(2000) Tyrosine phosphorylation in plant bending. Nature 407, 37.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
King JJ,
Stimart DP,
Fisher RH, Bleecker AB
(1995) A mutation altering auxin homeostasis and plant morphology in Arabidopsis. The Plant Cell 7, 2023–2037.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kohorn BD,
Kobayashi M,
Johansen S,
Riese J,
Huang LF,
Koch K,
Fu S,
Dotson A, Byers N
(2006) An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. The Plant Journal 46, 307–316.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Komis G,
Apostolakos P,
Gaitanaki C, Galatis B
(2004) Hyperosmotically induced accumulation of a phosphorylated p38-like MAPK involved in protoplast volume regulation of plasmolyzed wheat root cells. FEBS Letters 573, 168–174.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Konishi M, Sugiyama M
(2003) Genetic analysis of adventitious root formation with a novel series of temperature-sensitive mutants of Arabidopsis thaliana. Development 130, 5637–5647.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koontz DA, Choi JH
(1993) Protein phosphorylation in carrot somatic embryos in response to abscisic acid. Plant Physiology and Biochemistry 31, 95–102.
Lopez-Bucio J,
Cruz-Ramirez A, Herrera-Estrella L
(2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ludwig-Muller J,
Vertocnik A, Town CD
(2005) Analysis of indole-3-butyric acid induced adventitious root formation on Arabidopsis stem segments. Journal of Experimental Botany 56, 2095–2105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacRae TH
(1997) Tubulin post-translational modification-enzymes and their mechanisms of action. European Journal of Biochemistry 244, 265–278.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Malamy JN, Benfey PN
(1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33–44.
| PubMed |
Malamy JE, Ryan KS
(2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiology 127, 899–909.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Naska S,
Park KJ,
Hannigan GE,
Dedhar S,
Miller FD, Kaplan DR
(2006) An essential role for the integrin-linked kinase-glycogen synthase kinase-3 beta pathway during dendrite initiation and growth. Journal of Neuroscience 26, 13344–13356.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nishihama R,
Soyano T,
Ishikawa M,
Araki S, Tanaka H , et al.
(2002) Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109, 87–99.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Qian Y,
Zhong X,
Flynn DC,
Zheng JZ,
Qiao M,
Wu C,
Dedhar S,
Shi X, Jiang BH
(2005) ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 24, 3154–3165.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Raices M,
Gargantini PR,
Chinchilla D,
Crespi M,
Tellez-Inon MT, Ulloa RM
(2003) Regulation of CDPK isoforms during tuber development. Plant Molecular Biology 52, 1011–1024.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reddy MM, Rajasekharan R
(2006) Role of threonine residues in the regulation of manganese-dependent arabidopsis serine/threonine/tyrosine protein kinase activity. Archives of Biochemistry and Biophysics 455, 99–109.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reed RC,
Brady SR, Muday GK
(1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rodríguez-Zapata LC, Hernández-Sotomayor SM
(1997) Evidence of protein-tyrosine kinase activity in Catharanthus roseus roots transformed by Agrobacterium rhizogenes. Planta 204, 70–77.
| Crossref | GoogleScholarGoogle Scholar |
Rudrabhatla P,
Reddy MM, Rajasekharan R
(2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Molecular Biology 60, 293–319.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sakurai M,
Pak JY,
Muramatsu Y, Fukuhara T
(2004) Integrin-like protein at the invaginated plasma membrane of epidermal cells in mature leaves of the marine angiosperm Zostera marina L. Planta 220, 271–277.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sedgwick SG, Smerdon SJ
(1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends in Biochemical Sciences 24, 311–316.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smith RD, Walker JC
(1996) Plant protein phosphatases. Annual Review of Plant Physiology and Plant Molecular Biology 47, 101–125.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Szabados L,
Charrier B,
Kondorosi A,
de Bruijn FJ, Ratet P
(1995) New plant promoter and enhancer testing vectors. Molecular Breeding 1, 419–423.
| Crossref | GoogleScholarGoogle Scholar |
Tabe Y,
Jin L,
Satsuma-Ishii Y,
Xu Y, McQueen T , et al.
(2007) Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells. Cancer Research 67, 684–694.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tavares AA,
Glover DM, Sunkel CE
(1996) The conserved mitotic kinase polo is regulated by phosphorylation and has preferred microtubule-associated substrates in Drosophila embryo extracts. The EMBO Journal 15, 4873–4883.
| PubMed |
Taylor SS,
Knighton DR,
Zheng J,
Sowadski JM,
Gibbs CS, Zoller MJ
(1993) A template for the protein kinase family. Trends in Biochemical Sciences 18, 84–89.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tirichine L,
Imaizumi-Anraku H,
Yoshida S,
Murakami Y, Madsen LH , et al.
(2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tripp KW, Barrick D
(2007) Enhancing the stability and folding rate of a repeat protein through the addition of consensus repeats. Journal of Molecular Biology 365, 1187–1200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ullah H,
Chen JG,
Temple B,
Boyes DC,
Alonso JM,
Davis KR,
Ecker JR, Jones AM
(2003) The beta-subunit of the Arabidopsis G protein negatively regulates auxin induced cell division and affects multiple developmental processes. The Plant Cell 15, 393–409.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ulloa RM,
Torres HN,
Ochatt CM, Téllez-Iñón MT
(1991) Ca2+-Calmodulin dependent protein kinase activity in the ascomycetes Neurospora crassa. Molecular and Cellular Biochemistry 10, 155–163.
Vogel J,
Drapkin B,
Oomen J,
Beach D,
Bloom K, Snyder M
(2001) Phosphorylation of gamma-tubulin regulates microtubule organization in budding yeast. Developmental Cell 1, 621–631.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Whittington AT,
Vugrek O,
Wei KJ,
Hasenbein NG,
Sugimoto K,
Rashbrooke MC, Wasteneys GO
(2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411, 610–613.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wu C, Dedhar S
(2001) Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. Journal of Cell Biology 155, 505–510.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang T,
Du L, Poovaiah BW
(2007) Concept of redesigning proteins by manipulating calcium/calmodulin binding domains to engineer plants with altered traits. Functional Plant Biology 34, 343–352.
| Crossref | GoogleScholarGoogle Scholar |
Zhang H, Forde BG
(2000) Regulation of Arabidopsis root development by nitrate availability. Journal of Experimental Botany 51, 51–59.
| Crossref | GoogleScholarGoogle Scholar | PubMed |