Transcriptional control of aspartate kinase expression during darkness and sugar depletion in Arabidopsis: Involvement of bZIP transcription factors

Planta

Volumn 233, Issue 5, 2011, Pages 1025-1040

  Ufaz, Shai ^a   Shukla, Vijaya ^b   Soloveichik, Yulia ^a   Golan, Yelena ^a   Breuer, Frank ^b,c   Koncz, Zsuzsa ^b   Galili, Gad ^d   Koncz, Csaba ^b,e   Zilberstein, Aviah ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c The Weizmann Institute of Science ^*  (Germany)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

ABI5; Aspartate kinase; bZIP; DPBF4; SRDX; Sucrose

Indexed keywords

ARABIDOPSIS PROTEIN; ASPARTATE KINASE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; SUCROSE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; DARKNESS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PLANT GENE; PROMOTER REGION; REGULATORY SEQUENCE; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASPARTATE KINASE; BASE SEQUENCE; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DARKNESS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; MUTATION; PROMOTER REGIONS, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; SUCROSE; TRANSCRIPTIONAL ACTIVATION;

ARABIDOPSIS;

EID: 79954423811     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1360-9     Document Type: Article

References (64)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Alonso R, Oñate-Sánchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Dröge-Laser W (2009) A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21: 747-761.
3. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14: 2085-2096.
4. Arroyo A, Bossi F, Finkelstein RR, Leon P (2003) Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in Arabidopsis. Plant Physiol 133: 231-242.
5. Baena-González E (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3: 300-313.
6. Baena-González E, Sheen J (2008) Convergent energy and stress signalling. Trends Plant Sci 13: 474-482.
7. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938-942.
8. Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous DPBF1 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14: 1391-1403.
9. Bensmihen S, Giraudat J, Parcy F (2005) Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the DPBF1 family during Arabidopsis thaliana embryo maturation. J Exp Bot 56: 597-603.
10. Bhalerao R, Salchert K, Bakó L, Ökrész L, Szabados L, Muranaka T, Machida Y, Schell J, Koncz C (1999) Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc Natl Acad Sci USA 96: 5322-5327.
11. Bläsing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257-3281.
12. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39: 776-789.
13. Brocard IM, Lynch TJ, Finkelstein RR (2002) Regulation and role of the Arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiol 129: 1533-1543.
14. Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105: 4495-4500.
15. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
16. Craciun A, Jacobs M, Vauterin M (2000) Arabidopsis loss-of-function mutant in the lysine pathway points out complex regulation mechanisms. FEBS Lett 487: 234-238.
17. Curien G, Ravanel S, Robert M, Dumas R (2005) Identification of six novel allosteric effectors of Arabidopsis thaliana aspartate kinase-homoserine dehydrogenase isoforms; Physiological context sets the specificity. J Biol Chem 280: 41178-41183.
18. Curien G, Laurencin M, Robert-Genthon M, Dumas R (2007) Allosteric monofunctional aspartate kinases from Arabidopsis. FEBS J 274: 164-176.
19. Curien G, Bastien O, Robert-Genthon M, Cornish-Bowden A, Cárdenas ML, Dumas R (2009) Understanding the regulation of aspartate metabolism using a model based on measured kinetic parameters. Mol Syst Biol 5: 271.
20. Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, Vicente-Carbajosa J, Dröge-Laser W (2006) Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46: 890-900.
21. Farrás R, Ferrando A, Jásik J, Ökrész L, Tiburcio A, Salchert K, del Pozo C, Schell J, Koncz C (2001) SKP1-SnRK protein kinase mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 20: 2742-2756.
22. Ferrando A, Farrás R, Jasik J, Schell J, Koncz C (2000) Intron-tagged epitope: a tool for facile detection and purification of proteins expressed in Agrobacterium-transformed plant cells. Plant J 22: 553-560.
23. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609.
24. Finkelstein R, Gampala SS, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol Biol 59: 253-267.
25. Frankard V, Vauterin M, Jacobs M (1997) Molecular characterization of an Arabidopsis thaliana cDNA coding for a monofunctional aspartate kinase. Plant Mol Biol 34: 233-242.
26. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
27. Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7: 899-906.
28. Galili G (2002) New insights into the regulation and functional significance of lysine metabolism in plants. Annu Rev Plant Biol 53: 27-43.
29. Hanson J, Hanssen M, Wiese A, Hendriks MM, Smeekens S (2008) The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of asparagine synthetase 1 and proline dehydrogenase 2. Plant J 53: 935-949.
30. Hiratsu K, Ohta M, Matsui K, Ohme-Takagi M (2002) The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers. FEBS Lett 514: 351-354.
31. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733-739.
32. Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321: 172-178.
33. Jakoby M, Weisshaar B, Droege-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7: 106-111.
34. Jander G, Joshi V (2010) Recent progress in deciphering the biosynthesis of aspartate-derived amino acids in plants. Mol Plant 3: 54-65.
35. Kagale S, Links MG, Rozwadowski K (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152: 1109-1134.
36. Kang SG, Price J, Lin PC, Hong JC, Jang JC (2010) The Arabidopsis bZIP1 transcription factor is involved in sugar signaling, protein networking, and DNA binding. Mol Plant 3: 361-373.
37. Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11: 1237-1251.
38. Kim SY, Ma J, Perret P, Li Z, Thomas TL (2002) Arabidopsis DPBF1 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol 130: 688-697.
39. Koncz C, Martini N, Mayerhofer R, Koncz-Kalman Z, Körber H, Redei GP, Schell J (1989) High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci USA 86: 8467-8471.
40. Lam HM, Peng SSY, Coruzzi GM (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol 106: 1347-1357.
41. Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J 16: 345-353.
42. Less H, Galili G (2009) Coordinations between gene modules control the operation of plant amino acid metabolic networks. BMC Syst Biol 3: 14.
43. Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98: 4782-4787.
44. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32: 317-328.
45. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17: 410-418.
46. Matsui K, Ohme-Takagi M (2010) Detection of protein-protein interactions in plants using the transrepressive activity of the EAR motif repression domain. Plant J 61: 570-578.
47. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 106: 5418-5423.
48. Németh K, Salchert K, Putnoky P, Bhalerao R, Koncz-Kálmán Z, Stankovic-Stangeland B, Bakó L, Mathur J, Ökresz L, Stabel S, Geigenberger P, Stitt M, Rédei GP, Schell J, Koncz C (1998) Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev 12: 3059-3073.
49. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible WR (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49: 463-491.
50. Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16: 2128-2150.
51. Rognes SE, Dewaele E, Aas SF, Jacobs M, Frankard V (2003) Transcriptional and biochemical regulation of a novel Arabidopsis thaliana bifunctional aspartate kinase-homoserine dehydrogenase gene isolated by functional complementation of a yeast hom6 mutant. Plant Mol Biol 51: 281-294.
52. Schütze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13: 247-255.
53. Tang G, Zhu-Shimoni JX, Amir R, Zchori IB, Galili G (1997) Cloning and expression of an Arabidopsis thaliana cDNA encoding a monofunctional aspartate kinase homologous to the lysine-sensitive enzyme of Escherichia coli. Plant Mol Biol 34: 287-293.
54. Thum KE, Shasha DE, Lejay LV, Coruzzi GM (2003) Light- and carbon-signaling pathways. Modeling circuits of interactions. Plant Physiol 132: 440-452.
55. Thum KE, Shin MJ, Gutiérrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM (2008) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst Biol 2: 31.
56. Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146: 1834-1861.
57. Vauterin M, Frankard V, Jacobs M (1999) The Arabidopsis thalianaDHDPS gene encoding dihydrodipicolinate synthase, key enzyme of lysine biosynthesis, is expressed in a cell-specific manner. Plant Mol Biol 39: 695-708.
58. Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schütze K, Alonso R, Harter K, Vicente-Carbajosa J, Dröge-Laser W (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25: 3133-3143.
59. Wiese A, Elzinga N, Wobbes B, Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16: 1717-1729.
60. Yoshioka Y, Kurei S, Machida Y (2001) Identification of a monofunctional aspartate kinase gene of Arabidopsis thaliana with spatially and temporally regulated expression. Genes Genet Syst 76: 189-198.
61. Zhu-Shimoni JX, Galili G (1998) Expression of an Arabidopsis aspartate kinase/homoserine dehydrogenase gene is metabolically regulated by photosynthesis-related signals but not by nitrogenous compounds. Plant Physiol 116: 1023-1028.
62. Zhu-Shimoni JX, Lev-Yadun S, Matthews B, Galili G (1997) Expression of an aspartate kinase homoserine dehydrogenase gene is subject to specific spatial and temporal regulation in vegetative tissues, flowers, and developing seeds. Plant Physiol 113: 695-706.
63. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632.
64. Zuo J, Niu QW, Chua NH (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265-273.