GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana

Plant and Cell Physiology

Volumn 52, Issue 5, 2011, Pages 894-908

  Renault, Hugues ^a,b,e   El Amrani, Abdelhak ^b   Palanivelu, Ravishankar ^c,e   Updegraff, Emily P ^c   Yu, Agns ^d   Renou, Jean Pierre ^d   Preuss, Daphne ^c   Bouchereau, Alain ^a   Deleu, Carole ^a  

^a AGROCAMPUS OUEST   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITY OF CHICAGO   (United States)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

Arabidopsis thaliana; Cell elongation; Cell wall; GABA; Microarray; Secretory pathway

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 79956085832     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcr041     Document Type: Article

References (59)

1. Akama, K. and Takaiwa, F. (2007) C-terminal extension of rice glutam-ate decarboxylase (OsGAD2) functions as an autoinhibitory domain and overexpression of a truncated mutant results in the accumulation of extremely high levels of GABA in plant cells. J. Exp. Bot. 58: 2699-2707. (Pubitemid 47357568)
2. Arst, H.N. (1978) GABA transaminase provides an alternative route of b-alanine synthesis in Aspergillus nidulans. Mol. Gen. Genet. 163: 23-27.
3. Barker, J.L., Behar, T., Li, Y.X., Liu, Q.Y., Ma, W., Maric, D. et al. (1998) GABAergic cells and signals in CNS development. Perspect. Dev. Neurobiol. 5: 305-322. (Pubitemid 28505505)
4. Baum, G., Lev-Yadun, S., Fridmann, Y., Arazi, T., Katsnelson, H., Zik, M. et al. (1996) Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO J. 15: 2988-2996. (Pubitemid 26187747)
5. Beuve, N., Rispail, N., Laine, P., Cliquet, J.-B., Ourry, A. and Le Deunff, E. (2004) Putative role of g-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant, Cell and Environment 27: 1035-1046. (Pubitemid 39040300)
6. Binzel, M.L., Hasegawa, P.M., Rhodes, D., Handa, S., Handa, A.K. and Bressan, R.A. (1987) Solute accumulation in tobacco cells adapted to NaCl. Plant Physiol. 84: 1408-1415.
7. Bouché, N. and Fromm, H. (2004) GABA in plants: just a metabolite?. Trends Plant Sci. 9: 110-115. (Pubitemid 38300257)
8. Bouché, N., Lacombe, B. and Fromm, H. (2003) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol. 13: 607-610. (Pubitemid 37415024)
9. Boursiac, Y., Chen, S., Luu, D.-T., Sorieul, M., Van den Dries, N. and Maurel, C. (2005) Early effects of salinity on water transport in Arabidopsis roots. molecular and cellular features of aquaporin expression. Plant Physiol. 139: 790-805. (Pubitemid 43907107)
10. Bouzigues, C., Morel, M., Triller, A. and Dahan, M. (2007) Asymmetric redistribution of GABA receptors during GABA gradient sensing by nerve growth cones analyzed by single quantum dot imaging. Proc. Natl Acad. Sci. USA 104: 11251-11256. (Pubitemid 47175127)
11. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. et al. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510. (Pubitemid 32675716)
12. Chevrot, R., Rosen, R., Haudecoeur, E., Cirou, A., Shelp, B.J., Ron, E. et al. (2006) GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc. Natl Acad. Sci. USA 103: 7460-7464. (Pubitemid 43727855)
13. Cho, H.T. and Cosgrove, D.J. (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thali-ana. Proc. Natl Acad. Sci. USA 97: 9783-9788. (Pubitemid 30650853)
14. Chung, I., Bown, A.W. and Shelp, B.J. (1992) The production and efflux of 4-aminobutyrate in isolated mesophyll cells. Plant Physiol. 99: 659-664.
15. Cosgrove, D.J. (2000) Loosening of plant cell walls by expansins. Nature 407: 321-326.
16. Crawford, L.A., Bown, A.W., Breitkreuz, K.E. and Guinel, F.C. (1994) The synthesis of g-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol. 104: 865-871.
17. Crowe, M.L., Serizet, C., Thareau, V., Aubourg, S., Rouze, P., Hilson, P. et al. (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res. 31: 156-158. (Pubitemid 36150355)
18. Daniels, M.J., Mirkov, T.E. and Chrispeels, M.J. (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aqua-porin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol. 106: 1325-1333. (Pubitemid 24986557)
19. Fait, A., Fromm, H., Walter, D., Galili, G. and Fernie, A.R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13: 14-19.
20. Foerster, H.F. (1971) g-Aminobutyric acid as a required germinant for mutant spores of Bacillus megaterium. J. Bacteriol. 108: 817-823.
21. Gagnot, S., Tamby, J.-P., Martin-Magniette, M.-L., Bitton, F., Taconnat, L., Balzergue, S. et al. (2007) CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res. 36: D986-D990. (Pubitemid 351149857)
22. Ganguly, K., Schinder, A.F., Wong, S.T. and Poo, M.-M. (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105: 521-532. (Pubitemid 32520857)
23. Ge, S., Goh, E.L.K., Sailor, K.A., Kitabatake, Y., Ming, G. and Song, H. (2005) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593. (Pubitemid 43185382)
24. Ge, Y., Dudoit, S. and Speed, T.P. (2003) Resampling-based multiple testing for microarray data analysis. Test 12: 1-77. (Pubitemid 36964087)
25. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M. and Hofte, H. (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114: 295-305. (Pubitemid 28110919)
26. Handa, S., Bressan, R.A., Handa, A.K., Carpita, N.C. and Hasegawa, P.M. (1983) Solutes contributing to osmotic adjustment in cultured plant cells adapted to water stress. Plant Physiol. 73: 834-843.
27. Hepler, P.K., Vidali, L. and Cheung, A.Y. (2001) Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17: 159-187. (Pubitemid 33096174)
28. Hilson, P., Allemeersch, J., Altmann, T., Aubourg, S., Avon, A., Beynon, J. et al. (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res. 14: 2176-2189. (Pubitemid 39440201)
29. Kathiresan, A., Miranda, J., Chinnappa, C.C. and Reid, D.M. (1998) g-Aminobutyric acid promotes stem elongation in Stellaria long-ipes: the role of ethylene. Plant Growth Regul. 26: 131-137. (Pubitemid 28548230)
30. Kathiresan, A., Tung, P., Chinnappa, C.C. and Reid, D.M. (1997) g-Aminobutyric acid stimulates ethylene biosynthesis in sunflower. Plant Physiol. 115: 129-135. (Pubitemid 28378805)
31. Kinnersley, A.M. and Turano, F.J. (2000) g-Aminobutyric acid (GABA) and plant responses to stress. Crit. Rev. Plant Sci. 19: 479-509.
32. Lancien, M. and Roberts, M.R. (2006) Regulation of Arabidopsis thali-ana 14-3-3 gene expression by g-aminobutyric acid. Plant Cell Environ. 29: 1430-1436. (Pubitemid 43855759)
33. Lee, Y., Choi, D. and Kende, H. (2001) Expansins: ever-expanding numbers and functions. Curr. Opin. Plant Biol. 4: 527-532. (Pubitemid 33001803)
34. Lichtenthaler, H.K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148: 350-382.
35. Ludewig, F., Haùser, A., Fromm, H., Beauclair, L. and Bouché, N. (2008) Mutants of GABA transaminase (POP2) suppress the severe pheno-type of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis. PLoS ONE 3: e3383.
36. Lupo, M. and Halpern, Y.S. (1970) Gene controlling L-glutamic acid decarboxylase synthesis in Escherichia coli K-12. J. Bacteriol. 103: 382-386.
37. Lurin, C., Andres, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyere, C. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopep-tide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103. (Pubitemid 39059730)
38. Miyashita, Y. and Good, A.G. (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol. 49: 92-102.
39. Morse, D.E., Hooker, N., Duncan, H. and Jensen, L. (1979) g-Aminobutyric acid, a neurotransmitter, induces planktonic aba-lone larvae to settle and begin metamorphosis. Science 204: 407-410. (Pubitemid 9157302)
40. Mouille, G., Robin, S., Lecomte, M., Pagant, S. and Höfte, H. (2003) Classification and identification of Arabidopsis cell wall mutants using Fourier-Transform InfraRed (FT-IR) microspectroscopy. Plant J. 35: 393-404. (Pubitemid 36990641)
41. B receptor directly interacts with the activating transcription factor 4. J. Biol. Chem. 275: 35185-35185.
42. Owens, D.F. and Kriegstein, A.R. (2002) Is there more to GABA than synaptic inhibition?. Nat. Rev. Neurosci. 3: 715-727. (Pubitemid 135706677)
43. Palanivelu, R., Brass, L., Edlund, A.F. and Preuss, D. (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114: 47-59. (Pubitemid 36859840)
44. Park, D.H., Mirabella, R., Bronstein, P.A., Preston, G.M., Haring, M.A., Lim, C.K. et al. (2010) Mutations in g-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J. 64: 318-330.
45. Pinal, C.S. and Tobin, A.J. (1998) Uniqueness and redundancy in GABA production. Perspect. Dev. Neurobiol. 5: 109-118. (Pubitemid 28505489)
46. Reed, L.J. (1950) The occurrence of g-aminobutyric acid in yeast extract: its isolation and identification. J. Biol. Chem. 183: 451-458.
47. Refrégier, G., Pelletier, S., Jaillard, D. and Höfte, H. (2004) Interaction between wall deposition and cell elongation in dark-grown hypo-cotyl cells in Arabidopsis. Plant Physiol. 135: 959-968. (Pubitemid 38819039)
48. Renault, H., Roussel, V., El Amrani, A., Arzel, M., Renault, D., Bouchereau, A. et al. (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10: 20.
49. Represa, A. and Ben-Ari, Y. (2005) Trophic actions of GABA on neur-onal development. Trends Neurosci. 28: 278-283. (Pubitemid 40775771)
50. Roberts, E. and Frankel, S. (1950) g-Aminobutyric acid in brain: its formation from glutamic acid. J. Biol. Chem. 187: 55-63.
51. Roberts, M.R. (2007) Does GABA act as a signal in plants? Hints from molecular studies. Plant Signa. Behav. 2: 408-409. (Pubitemid 350124675)
52. Solomon, P.S. and Oliver, R.P. (2001) The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213: 241-249. (Pubitemid 32623581)
53. Steward, F.C., Thompson, J.F. and Dent, C.E. (1949) g-Aminobutyric acid: a constituent of the potato tuber?. Science 110: 439-440.
54. Tokunaga, M., Nakano, Y. and Kitaoka, S. (1979) Subcellular localization of the GABA-shunt enzymes in Euglena gracilis strain Z. J. Eurkaryot. Microbiol. 26: 471-473.
55. Van Hengel, A.J., Barber, C. and Roberts, K. (2004) The expression patterns of arabinogalactan-protein AtAGP30 and GLABRA2 reveal a role for abscisic acid in the early stages of root epidermal patterning. Plant J. 39: 70-83. (Pubitemid 38893579)
56. Van Hengel, A.J. and Roberts, K. (2003) AtAGP30, an arabinogalactan- protein in the cell walls of the primary root, plays a role in root regeneration and seed germination. Plant J. 36: 256-270. (Pubitemid 37293065)
57. B receptor interacts directly with the related transcription factors CREB2 and ATFx. Proc. Natl Acad. Sci. USA 97: 13967-13967.
58. Wilhelmi, L.K. and Preuss, D. (1996) Self-sterility in Arabidopsis due to defective pollen tube guidance. Science 274: 1535-1537. (Pubitemid 26403930)
59. Yamaguchi-Shinozaki, K., Koizumi, M., Urao, S. and Shinozaki, K. (1992) Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: sequence analysis of one cDNA clone that encodes a putative trans-membrane channel protein. Plant Cell Physiol. 33: 217-224.