Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family

Plant Physiology

Volumn 143, Issue 2, 2007, Pages 941-958

  Manfield, Iain W ^a   Devlin, Paul F ^b   Jen, Chih Hung ^a,c   Westhead, David R ^a   Gilmartin, Philip M ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; MICROARRAYS; MUTAGENESIS; PROTEINS; TISSUE; TRANSCRIPTION;

GATA TRANSCRIPTION; SUSPENSION CELL CULTURES;

PLANTS (BOTANY);

PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; TRANSCRIPTION FACTOR GATA; ZINC FINGER PROTEIN;

ANTIBODY SPECIFICITY; ARABIDOPSIS; ARTICLE; CIRCADIAN RHYTHM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; LIGHT; METABOLISM; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN MOTIF; RADIATION EXPOSURE;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CIRCADIAN RHYTHM; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LIGHT; MULTIGENE FAMILY; ORGAN SPECIFICITY; VARIATION (GENETICS); ZINC FINGERS;

EID: 34247184185     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.106.090761     Document Type: Article

References (84)

1. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815
2. Arguello-Astorga G, Herrera-Estrella L (1998) Evolution of light-regulated plant promoters. Annu Rev Plant Physiol Plant Mol Biol 49: 525-555
3. Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, Macino G (1996) White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J 15: 1650-1657
4. Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S (2005) Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. Plant J 44: 680-692
5. Bonaventure G, Ohlrogge JB (2002) Differential regulation of mRNA levels of acyl carrier protein isoforms in Arabidopsis. Plant Physiol 128: 223-235
6. Borello U, Ceccarelli E, Giuliano G (1993) Constitutive, light-responsive and circadian clock-responsive factors compete for the different L-box elements in plant light-regulated promoters. Plant J 4: 611-619
7. Buzby JS, Yamada T, Tobin EM (1990) A light-regulated DNA-binding activity interacts with a conserved region of a Lemna gibba-rbcS promoter. Plant Cell 2: 805-814
8. Carré IA, Kay SA (1995) Multiple DNA-protein complexes at a circadian-regulated promoter element. Plant Cell 7: 2039-2051
9. Casneuf T, De Bodt S, Raes J, Maere S, Van de Peer Y (2006) Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol 7: R13
10. Castresana C, Garcia-Luque I, Alonso E, Malik VS, Cashmore AR (1988) Both positive and negative regulatory elements mediate expression of a photoregulated Cab gene from Nicotiana plumbaginifolia. EMBO J 7: 1929-1936
11. Causier B, Castillo R, Zhou JL, Ingram R, Xue YB, Schwarz-Sommer Z, Davies B (2005) Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15: 1508-1512
12. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87-117
13. Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38: 332-347
14. Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S (2004) NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32: D575-D577
15. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38: 366-379
16. Daniel-Vedele F, Caboche M (1993) A tobacco cDNA clone encoding a GATA-1 zinc finger protein homologous to regulators of nitrogen metabolism in fungi. Mol Gen Genet 240: 365-373
17. Dean C, van den Elzen P, Tamaki S, Dunsmuir P, Bedbrook J (1985) Differential expression of the 8 genes of the Petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J 4: 3055-3061
18. Dickey LF, Petracek ME, Sowinski DA, Hansen ER, Nguyen TT, Allen GC, Thompson WF (1997) Light effects on ferredoxin mRNA stability are mediated by translation. Plant Physiol 114: 1213-1227
19. Donald RGK, Cashmore AR (1990) Mutation of either G-Box or I-Box sequences profoundly affects expression from the Arabidopsis Rbcs-1a promoter. EMBO J 9: 1717-1726
20. Eastmond PJ, Germain V, Lange PR, Bryce JH, Smith SM, Graham IA (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc Natl Acad Sci USA 97: 5669-5674
21. Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JCW, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18: 639-650
22. Evans T, Felsenfeld G (1989) The erythroid-specific transcription factor Eryf1: a new finger protein. Cell 58: 877-885
23. Evans T, Reitman M, Felsenfeld G (1988) An erythrocyte-specific DNA-binding factor recognizes a regulatory sequence common to all chicken globin genes. Proc Natl Acad Sci USA 85: 5976-5980
24. Fu YH, Marzluf GA (1990) Site-directed mutagenesis of the zinc finger DNA-binding domain of the nitrogen-regulatory protein Nit2 of Neurospora. Mol Microbiol 4: 1847-1852
25. Gidoni D, Brosio P, Bond-Nutter D, Bedbrook J, Dunsmuir P (1989) Novel cis-acting elements in Petunia Cab gene promoters. Mol Gen Genet 215: 337-344
26. Gilmartin PM, Sarokin L, Memelink J, Chua NH (1990) Molecular light switches for plant genes. Plant Cell 2: 369-378
27. Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein-binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85: 7089-7093
28. Griffiths S, Dunford R, Coupland G, Laurie D (2003) The evolution of CONSTANS-like gene families in barley, rice and Arabidopsis. Plant Physiol 131: 1855-1867
29. Grob U, Stuber K (1987) Discrimination of phytochrome dependent light inducible from non-light inducible plant genes: prediction of a common light-responsive element (Lre) in phytochrome dependent light inducible plant genes. Nucleic Acids Res 15: 9957-9973
30. Gualberti G, Papi M, Bellucci L, Ricci L, Bouchez D, Camilleri C, Costantino P, Vittorioso P (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14: 1253-1263
31. Hadden DA, Phillipson BA, Johnston KA, Brown L-A, Manfield IW, El-Shami M, Sparkes IA, Baker A (2006) Arabidopsis PEX19 is a dimeric protein that binds the peroxin PEX10. Mol Membr Biol 23: 325-336
32. Hansen ER, Petracek ME, Dickey LF, Thompson WF (2001) The 5′ end of the pea ferredoxin-1 mRNA mediates rapid and reversible light-directed changes in translation in tobacco. Plant Physiol 125: 770-778
33. Harmer SL, Hogenesch LB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113
34. Jen CH, Manfield IW, Michalopoulos I, Pinney JW, Willats WGT, Gilmartin PM, Westhead DR (2006) The Arabidopsis co-expression tool (ACT): a WWW-based tool and database for microarray-based gene expression analysis. Plant J 46: 336-348
35. Jeong MJ, Shih MC (2003) Interaction of a GATA factor with cis-acting elements involved in light regulation of nuclear genes encoding chloroplast glyceraldehyde-3-phosphate dehydrogenase in Arabidopsis. Biochem Biophys Res Commun 300: 555-562
36. Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 33: 955-965
37. Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T (2005) Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His -> Asp phosphorelay circuitry. Plant Cell Physiol 46: 339-355
38. Kikis EA, Khanna R, Quail PH (2005) ELF4 is a phytochrome- regulated component of a negative feedback loop involving the central oscillator components CCA1 and LHY. Plant J 44: 300-313
39. Kozak M (2000) Do the 5′ untranslated domains of human cDNAs challenge the rules for initiation of translation (or is it vice versa)? Genomics 70: 396-406
40. Kudla B, Caddick MX, Langdon T, Martinez-Rossi NM, Bennett CF, Sibley S, Davies RW, Arst HN (1990) The regulatory gene AreA mediating nitrogen metabolite repression in Aspergillus nidulans - mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J 9: 1355-1364
41. Lam E, Chua NH (1989) ASF-2: a factor that binds to the cauliflower mosaic virus-35S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1: 1147-1156
42. Lam E, Kano-Murakami Y, Gilmartin P, Niner B, Chua NH (1990) A metal-dependent DNA-binding protein interacts with a constitutive element of a light-responsive promoter. Plant Cell 2: 857-866
43. Ledger S, Strayer C, Ashton F, Kay SA, Putterill J (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 26: 14-22
44. Linden H, Macino G (1997) White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J 16: 98-109
45. Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (blue micropylar end 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J 44: 960-971
46. Lowry JA, Atchley WR (2000) Molecular evolution of the GATA family of transcription factors: conservation within the DNA-binding domain. J Mol Evol 50: 103-115
47. Manfield IW, Jen C-H, Pinney JW, Michalopoulos I, Bradford JR, Gilmartin PM, Westhead DR (2006) Arabidopsis co-expression tool (ACT): web server tools for microarray-based gene expression analysis. Nucleic Acids Res 34: W504-W509
48. Manfield IW, Reynolds LA, Gittins J, Kneale GG (2000) The DNA-binding domain of the gene regulatory protein AreA extends beyond the minimal zinc-finger region conserved between GATA proteins. Biochim Biophys Acta 1493: 325-332
49. Merika M, Orkin SH (1993) DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 13: 3999-4010
50. Meyers BC, Vu TH, Tej SS, Ghazal H, Matvienko M, Agrawal V, Ning JC, Haudenschild CD (2004) Analysis of the transcriptional complexity of Arabidopsis thaliana by massively parallel signature sequencing. Nat Biotechnol 22: 1006-1011
51. Millar AJ, Carré IA, Strayer CA, Chua NH, Kay SA (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267: 1161-1163
52. Monte E, Tepperman JM, Al-Sady B, Kaczorowski KA, Alonso JM, Ecker JR, Li X, Zhang YL, Quail PH (2004) The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc Natl Acad Sci USA 101: 16091-16098
53. Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20: 8635-8642
54. Nemoto Y, Kisaka M, Fuse T, Yano M, Ogihara Y (2003) Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J 36: 82-93
55. Newman TC, Ohme-Takagi M, Taylor CB, Green PJ (1993) DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5: 701-714
56. Nishii A, Takemura M, Fujita H, Shikata M, Yokota A, Kohchi T (2000) Characterization of a novel gene encoding a putative single zinc-finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana. Biosci Biotechnol Biochem 64: 1402-1409
57. Oh E, Kim J, Park E, Kim JI, Kang C, Choi G (2004) PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16: 3045-3058
58. Omichinski JG, Clore GM, Schaad O, Felsenfeld G, Trainor C, Appella E, Stahl SJ, Gronenborn AM (1993) NMR structure of a specific DNA complex of Zn-containing DNA-binding domain of GATA-1. Science 261: 438-446
59. Orkin SH (1992) GATA-binding transcription factors in hematopoietic cells. Blood 80: 575-581
60. Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15: 1998-2006
61. Persson S, Wei HR, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102: 8633-8638
62. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc-finger transcription factors. Cell 80: 847-857
63. Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134: 1718-1732
64. Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110
65. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In S Krawetz, S Misener, eds, Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ, pp 365-386
66. Sarokin LP, Chua NH (1992) Binding-sites for 2 novel phosphoproteins, 3AF5 and 3AF3, are required for Rbcs-3a expression. Plant Cell 4: 473-483
67. Scazzocchio C (2000) The fungal GATA factors. Curr Opin Microbiol 3: 126-131
68. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93: 1219-1229
69. Schindler U, Cashmore AR (1990) Photoregulated gene-expression may involve ubiquitous DNA-binding proteins. EMBO J 9: 3415-3427
70. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506
71. Shen H, Moon J, Huq E (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44: 1023-1035
72. Shikata M, Matsuda Y, Ando K, Nishii A, Takemura M, Yokota A, Kohchi T (2004) Characterization of Arabidopsis ZIM, a member of a novel plantspecific GATA factor gene family. J Exp Bot 55: 631-639
73. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and post-transcriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136: 2687-2699
74. Sugimoto K, Takeda S, Hirochika H (2003) Transcriptional activation mediated by binding of a plant GATA-type zinc finger protein AGP1 to the AG-motif (AGATCCAA) of the wound-inducible Myb gene NtMyb2. Plant J 36: 550-564
75. Teakle GR, Gilmartin PM (1998) Two forms of type IV zinc-finger motif and their kingdom-specific distribution between the flora, fauna and fungi. Trends Biochem Sci 23: 100-102
76. Teakle GR, Kay SA (1995) The GATA-binding protein CGF-1 is closely related to GT-1. Plant Mol Biol 29: 1253-1266
77. Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50: 43-57
78. Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci USA 98: 9437-9442
79. Tsai SF, Martin DI, Zon LI, D'Andrea AD, Wong GG, Orkin SH (1989) Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature 339: 446-451
80. Umemura Y, Ishiduka T, Yamamoto R, Esaka M (2004) The Dof domain, a zinc finger DNA-binding domain conserved only in higher plants, truly functions as a Cys2/Cys2 Zn finger domain. Plant J 37: 741-749
81. Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9: 491-507
82. 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
83. Zhao YX, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 16: 2586-2600
84. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632