Glutamate signalling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture

Plant Journal

Volumn 75, Issue 1, 2013, Pages 1-10

  Forde, Brian G ^a   Cutler, Sean R ^b   Zaman, Najia ^c   Krysan, Patrick J ^c  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

amino acids; Arabidopsis thaliana L.; chemical genetics; MAP kinase; nutrient signalling; roots; Saccharomyces cerevisiae; signal transduction

Indexed keywords

ARABIDOPSIS ROOTS; ARABIDOPSIS THALIANA; ARABIDOPSIS THALIANA L; CHEMICAL GENETICS; KINASE-DEPENDENT PATHWAY; MAP KINASE; ROOTS; SIGNALLING PATHWAYS;

AMINO ACIDS; ARCHITECTURE; ENZYMES; MAMMALS; SIGNAL TRANSDUCTION;

YEAST;

2 PYRROLIDONE DERIVATIVE; AMINO ACID; ARABIDOPSIS PROTEIN; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; THIOCYANIC ACID DERIVATIVE;

ARABIDOPSIS; ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR LIBRARY; MUTATION; PHYSIOLOGY; PLANT ROOT; SACCHAROMYCES CEREVISIAE; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GLUTAMIC ACID; MAP KINASE KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MUTATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PYRROLIDINONES; SACCHAROMYCES CEREVISIAE; SEEDLING; SMALL MOLECULE LIBRARIES; THIOCYANATES;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84879245087     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12201     Document Type: Article

References (49)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Berger, F., Linstead, P., Dolan, L., and, Haseloff, J., (1998) Stomata patterning on the hypocotyl of Arabidopsis thaliana is controlled by genes involved in the control of root epidermis patterning. Dev. Biol. 194, 226-234.
3. Bush, S.M., and, Krysan, P.J., (2010) iTILLING: a personalized approach to the identification of induced mutations in Arabidopsis. Plant Physiol. 154, 25-35.
4. Champion, A., Picaud, A., and, Henry, Y., (2004) Reassessing the MAP3K and MAP4K relationships. Trends Plant Sci. 9, 123-129.
5. Chiu, J.C., Brenner, E.D., DeSalle, R., Nitabach, M.N., Holmes, T.C., and, Coruzzi, G.M., (2002) Phylogenetic and expression analysis of the glutamate receptor-like gene family in Arabidopsis thaliana. Mol. Biol. Evol. 19, 1066-1082.
6. Demidchik, V., Essah, P.A., and, Tester, M., (2004) Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta, 219, 167-175.
7. Dubos, C., Huggins, D., Grant, G.H., Knight, M.R., and, Campbell, M.M., (2003) A role for glycine in the gating of plant NMDA-like receptors. Plant J. 35, 800-810.
8. Forde, B.G., and, Lea, P.J., (2007) Glutamate in plants: metabolism, regulation and signalling. J. Exp. Bot. 58, 2339-2358.
9. Fukunaga, K., and, Miyamoto, E., (1998) Role of MAP kinase in neurons. Mol. Neurobiol. 16, 79-95.
10. Gao, M.H., Liu, J.M., Bi, D.L., Zhang, Z.B., Cheng, F., Chen, S.F., and, Zhang, Y.L., (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190-1198.
11. Garcia, S., Lopez, E., and, Lopez-Colome, A.M., (2008) Glutamate accelerates RPE cell proliferation through ERK1/2 activation via distinct receptor-specific mechanisms. J. Cell. Biochem. 104, 377-390.
12. Gomez-Gomez, L., Felix, G., and, Boller, T., (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277-284.
13. Haddad, J.J., (2005) N-methyl-D-aspartate (NMDA) and the regulation of mitogen-activated protein kinase (MAPK) signaling pathways: a revolving neurochemical axis for therapeutic intervention? Prog. Neurobiol. 77, 252-282.
14. Ichimura, K., Shinozaki, K., Tena, G., et al. (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308.
15. Ichimura, K., Casais, C., Peck, S.C., Shinozaki, K., and, Shirasu, K., (2006) MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J. Biol. Chem. 281, 36969-36976.
16. Ide, K., Takahashi, K., Nakano, T., Sato, M., and, Omori, M., (2006) Chemoreceptive foraging in a shallow-water scavenging lysianassid amphipod: role of amino acids in the location of carrion in Scopelocheirus onagawae. Mar. Ecol. Prog. Ser. 317, 193-202.
17. Kitagawa, T., Hashizume, Y., Murakane, T., et al. (2007) Screening of drugs that suppress Ste11 MAPKKK activation in yeast identified a c-Abl tyrosine kinase inhibitor. Biosci. Biotechnol. Biochem. 71, 772-782.
18. Kong, Q., Qu, N., Gao, M.H., et al. (2012) The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell, 24, 2225-2236.
19. Kwaaitaal, M., Huisman, R., Maintz, J., Reinstadler, A., and, Panstruga, R., (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440, 355-365.
20. Lam, H.-M., Chiu, J., Hsieh, M.-H., Meisel, L., Oliveira, I.C., Shin, M., and, Coruzzi, G., (1998) Glutamate receptor genes in plants. Nature, 396, 125-126.
21. Lux, R., and, Shi, W.Y., (2004) Chemotaxis-guided movements in bacteria. Crit. Rev. Oral Biol. Med. 15, 207-220.
22. Mao, L.M., Tang, Q.S., Samdani, S., Liu, Z.G., and, Wang, J.Q., (2004) Regulation of MAPK/ERK phosphorylation via ionotropic glutamate receptors in cultured rat striatal neurons. Eur. J. Neurosci. 19, 1207-1216.
23. Meyerhoff, O., Muller, K., Roelfsema, M., Latz, A., Lacombe, B., Hedrich, R., Dietrich, P., and, Becker, D., (2005) AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta, 222, 418-427.
24. Miao, Y., Laun, T.M., Smykowski, A., and, Zentgraf, U., (2007) Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol. Biol. 65, 63-76.
25. 2+ channels in pollen tubes and are regulated by pistil D-serine. Science, 332, 434-437.
26. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., YamaguchiShinozaki, K., Matsumoto, K., and, Shinozaki, K., (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 93, 765-769.
27. Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V., and, Hirt, H., (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697-38704.
28. Nobbe, F., (1862) Uber die feinere Verästelung der Pflanzenwurzeln. Landwirtschaftlichen Versuchs-Stationen, 4, 212-224.
29. Qi, Z., Stephens, N.R., and, Spalding, E.P., (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol. 142, 963-971.
30. Rasmussen, M., Roux, M., Petersen, M., and, Mundy, J., (2012) MAP kinase cascades in Arabidopsis innate immunity. Front. Plant Sci. 3, 169.
31. Robinson, D., (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol. 127, 635-674.
32. Rodriguez, M.C.S., Petersen, M., and, Mundy, J., (2010) Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649.
33. Rothstein, D.E., (2009) Soil amino-acid availability across a temperate-forest fertility gradient. Biogeochemistry, 92, 201-215.
34. Ruzicka, K., Simaskova, M., Duclercq, J., Petrasek, J., Zazimalova, E., Simon, S., Friml, J., Van Montagu, M.C.E., and, Benkova, E., (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl Acad. Sci. USA, 106, 4284-4289.
35. Schimel, J.P., and, Bennett, J., (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology, 85, 591-602.
36. Sivaguru, M., Pike, S., Gassmann, W., and, Baskin, T.I., (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol. 44, 667-675.
37. Stephens, N.R., Qi, Z., and, Spalding, E.P., (2008) Glutamate receptor subtypes evidenced by differences in desensitization and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol. 146, 529-538.
38. Su, S.H., Bush, S.M., Zaman, N., Stecker, K., Sussman, M.R., and, Krysan, P.J., (2013) Upregulation of the Arabidopsis MAP kinase kinase kinase MEKK2 is responsible for the autoimmune phenotypes of mekk1, mkk1 mkk2, and mpk4 mutant plants. Plant Cell (in press).
39. Su, S.H., Suarez-Rodriguez, M.C., and, Krysan, P., (2007) Genetic interaction and phenotypic analysis of the Arabidopsis MAP kinase pathway mutations mekk1 and mpk4 suggests signaling pathway complexity. FEBS Lett. 581, 3171-3177.
40. Suarez-Rodriguez, M.C., Adams-Phillips, L., Liu, Y.D., Wang, H.C., Su, S.H., Jester, P.J., Zhang, S.Q., Bent, A.F., and, Krysan, P.J., (2007) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143, 661-669.
41. Teardo, E., Segalla, A., Formentin, E., Zanetti, M., Marin, O., Giacometti, G.M., Lo Schiavo, F., Zoratti, M., and, Szabo, I., (2010) Characterization of a plant glutamate receptor activity. Cell. Physiol. Biochem. 26, 253-262.
42. Toth, R., and, van der Hoorn, R.A.L., (2010) Emerging principles in plant chemical genetics. Trends Plant Sci. 15, 81-88.
43. Turano, F.J., Panta, G.R., Allard, M.W., and, van Berkum, P., (2001) The putative glutamate receptors from plants are related to two superfamilies of animal neurotransmitter receptors via distinct evolutionary mechanisms. Mol. Biol. Evol. 18, 1417-1420.
44. 2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol. 159, 40-46.
45. Walch-Liu, P., and, Forde, B.G., (2007) L-Glutamate as a novel modifier of root growth and branching: What's the sensor? Plant Signal. Behav. 2, 284-286.
46. Walch-Liu, P., and, Forde, B.G., (2008) Nitrate signaling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. Plant J. 54, 820-828.
47. Walch-Liu, P., Liu, L.-H., Remans, T., Tester, M., and, Forde, B.G., (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol. 47, 1045-1057.
48. Wang, J.Q., Fibuch, E.E., and, Mao, L.M., (2007) Regulation of mitogen-activated protein kinases by glutamate receptors. J. Neurochem. 100, 1-11.
49. Watkins, J.C., and, Jane, D.E., (2006) The glutamate story. Br. J. Pharmacol. 147, S100-S108.