The Arabidopsis zinc finger-homeodomain genes encode proteins with unique biochemical properties that are coordinately expressed during floral development

Plant Physiology

Volumn 140, Issue 3, 2006, Pages 1095-1108

  Tan, Queenie K G ^a,b   Irish, Vivian F ^a  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENES; PROTEINS; TISSUE; ZINC;

ARABIDOPSIS; BIOCHEMICAL PROPERTIES; FLORAL TISSUE; HOMEOBOX GENES;

GENETIC ENGINEERING;

GENES; NUCLEIC ACIDS; PLANT TISSUES; PROTEINS; ZINC;

ARABIDOPSIS; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS PROTEIN; HOMEODOMAIN PROTEIN; ZINC FINGER PROTEIN;

ARABIDOPSIS; ARTICLE; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE; TWO HYBRID SYSTEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE; TWO-HYBRID SYSTEM TECHNIQUES; ZINC FINGERS;

EID: 33646904813     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.070565     Document Type: Article

References (85)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Baima S, Nobili F, Sessa G, Lucchetii S, Ruberti I, Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171-4182
3. Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G (2001) The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126: 643-655
4. Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis ihaliana: an analysis of development in ihe wild type and in the shoot meristemless mutant. Development 119: 823-831
5. Baum SF, Eshed Y, Bowman JL (2001) The Arabidopsis nectary is an ABC-independent floral structure. Development 128: 4657-4667
6. Biggin MD, Tjian R (1989) A purified Drosophila homeodomain protein represses transcription in vitro. Cell 58: 433-440
7. Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13: 137-144
8. Bowman JL (2000) The YABBY gene family and abaxial cell fate. Curr Opin Plant Biol 3: 17-22
9. Bowman JL (2004) Class III HD-zip gene regulation, the golden fleece of ARGONAUTE activity? Bioessays 26: 938-942
10. Brazma A, Parkinson H, Sarkans U, Shojatalab M, ViIo J, Abeygunawardena N, Holloway E, Kapushenksy M, Kemmeren P, Lara GG, et al (2003) ArrayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res 31: 68-71
11. Burglin TR (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res 25: 4173-4180
12. Chan RL, Gago GM, Palena CM, Gonzalez DH (1998) Homeoboxes in plant development. Biochim Biophys Acta 1442: 1-19
13. Chariot A, Gielen J, Merville MP, Bours V (1999) The homeodomain- containing proteins: an update on their interacting partners. Biochem Pharmacol 58: 1851-1857
14. Chuck G, Lincoln C, Hake S (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8: 1277-1289
15. Connolly JP, Augustine JG, Francklyn C (1999) Mutational analysis of the engrailed homeodomain recognition helix by phage display. Nucleic Acids Res 27: 1182-1189
16. 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 Acid Res 32: D575-D577
17. Curtiss J, Heilig JS (1998) DeLIMiting development. Bioessays 20: 58-69
18. Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14: 547-558
19. Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCB1 gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
20. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANAD1 genes. Curr Biol 13: 1768-1774
21. Foster T, Yamaguchi J, Wong BC, Veit B, Hake S (1999) Gnarleyl is a dominant mutation in the knox4 homeobox gene affecting cell shape and identity. Plant Cell 11: 1239-1252
22. Fraenkel E, Pabo CO (1998) Comparison of x-ray and NMR structures for the Antennapedia homeodomain-DNA complex. Nat Struct Biol 5: 692-697
23. Gehring WJ, Affolter M, Burglin T (1994) Homeodomain proteins. Annu Rev Biochem 63: 487-526
24. Hackbusch J, Richter K, Muller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102: 4908-4912
25. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657-668
26. Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20: 125-151
27. Hill T, Day CD, Zondlo SC, Thackeray A, Irish VF (1998) Transcriptional regulation of the Arabidopsis floral homeotic gene APETALA3 is mediated by discrete spatial and temporal cis-acting elements. Development 125: 1711-1721
28. Hirsch JA, Aggarwal AK (1995) Structure of the even-skipped homeodomain complexed to AT-rich DNA: new perspectives on homeodomain specificity. EMBO J 14: 6280-6291
29. Innis MA, Gelfand DH, Sninsky JJ, White TJ (1990) PCR Protocols: A Guide to Methods and Applications. San Diego Academic Press, San Diego
30. Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405-413
31. Jin Y, Zhong H, Vershon AK (1999) The yeast a1 and alpha2 homeodomain proteins do not contribute equally to heterodimeric DNA binding. Mol Cell Biol 19: 585-593
32. Kawata H, Yamada K, Shou Z, Mizutani T, Miyamoto K (2003) The mouse zinc-fingers and homeoboxes (ZHX) family; ZHX2 forms a heterodimer with ZHX3. Gene 323: 133-140
33. Kissinger CR, Liu BS, Martin-Blanco E, Kornberg TB, Pabo CO (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63: 579-590
34. Klemm JD, Rould MA, Aurora R, Herr W, Pabo CO (1994) Crystal structure of the Oci-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules. Cell 77: 21-32
35. Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87-96
36. Lenhard M, Bohnert A, Jurgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814
37. Li T, Stark MR, Johnson AD, Wolberger C (1995) Crystal structure of the MATa1/MAT alpha 2 homeodomain heterodimer bound to DNA. Science 270: 262-269
38. Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859-1876
39. Lohmann JTJ, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral pattern-ing in Arabidopsis. Cell 105: 793-803
40. Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69
41. Maddison WP, Maddison DR (1989) Interactive analysis of phylogeny and character evolution using the computer program MacClade. Folia Primatol (Basel) 53: 190-202
42. Mann RS (1995) The specificity of homeotic gene function. Bioessays 17: 855-863
43. Matsumoto N, Okada K (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 15: 3355-3364
44. Matsumoto K, Tanaka T, Furuyama T, Kashihara Y, Mori T, Ishii N, Kitanaka J, Takemura M, Tohyama M, Wanaka A (1996) L3, a novel murine LIM-homeodomain transcription factor expressed in the ventral telencephalon and the mesenchyme surrounding the oral cavity. Neurosci Lett 204: 113-116
45. McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935-2942
46. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709-713
47. McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ (1984a) A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37: 403-408
48. McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ (1984b) A conserved DNA sequence in homoeotic genes of the Drosophila antennapedia and bithorax complexes. Nature 308: 428-433
49. Mead J, Zhong H, Acton TB, Vershon AK (1996) The yeast alpha2 and Mcml proteins interact through a region similar to a motif found in homeodomain proteins of higher eukaryotes. Mol Cell Biol 16: 2135-2143
50. Mele G, Ori N, Sato Y, Hake S (2003) The knottedl-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17: 2088-2093
51. Meyers BC, Lee DK, Vu TH, Tej SS, Edberg SB, Matvienko M, Tindell LD (2004) Arabidopsis MPSS: an online resource for quantitative expression analysis. Plant Physiol 135: 801-813
52. Muller KJ, Romano N, Gerstner O, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (1995) The barley hooded mutation caused by a duplication in a homeobox gene intron. Nature 374: 727-730
53. Nepveu A (2001) Role of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development. Gene 270: 1-15
54. Nishimura A, Tamaoki M, Sakamoto T, Matsuoka M (2000) Over-expression of tobacco knottedl-type class1 homeobox genes alters various leaf morphology. Plant Cell Physiol 41: 583-590
55. Ohashi-Ito K, Fukuda H (2003) HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44: 1350-1358
56. Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25: 223-236
57. Passner JM, Ryoo HD, Shen L, Mann RS, Aggarwal AK (1999) Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 397: 714-719
58. Peltenburg LT, Murre C (1997) Specific residues in the Pbx homeodomain differentially modulate the DNA-binding activity of Hox and Engrailed proteins. Development 124: 1089-1098
59. Pinsonneault J, Florence B, Vaessin H, McGinnis W (1997) A model for extradenticle function as a switch that changes HOX proteins from repressors to activators. EMBO J 16: 2032-2042
60. Piper DE, Batchelor AH, Chang CP, Cleary ML, Wolberger C (1999) Structure of a HoxB1-Pbx1 heterodtmer bound to DNA: role of the hexapeptide and a fourth homeodomain helix in complex formation. Cell 96: 587-597
61. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61-76
62. Riechmann JL (2002) Transcriptional regulation: a genomic overview. In CR Somerville, EM Meyerowitz, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, doi/10.1199/tab.0085, http://www.aspb.org/ publications/arabidopsis/
63. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Biomformatics 19: 1572-1574
64. Sato Y, Sentoku N, Miura Y, Hirochika H, Kitano H, Matsuoka M (1999) Loss-of-function mutations in the rice homeobox gene OSH15 affect the architecture of internodes resulting in dwarf plants. EMBO J 18: 992-1002
65. Scott MP, Weiner AJ (1984) Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci USA 81: 4115-4119
66. Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38: 609-622
67. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994
68. Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeo box gene, KNOTTED-I, causes a switch from determinate to indeterminate cell fates. Genes Dev 7: 787-795
69. Smith DL, Johnson AD (1992) A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an alpha 2 dimer. Cell 68: 133-142
70. Smith LG, Greene B, Veit B, Hake S (1992) A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116: 21-30
71. Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, MA
72. Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54: 582-596
73. Talbert PB, Adler HT, Parks DW, Comai L (1995) The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121: 2723-2735
74. Tan S, Richmond TJ (1998) Crystal structure of the yeast MATalpha2/MCM1/DNA ternary complex. Nature 391: 660-666
75. Tucker SC, Wisdom R (1999) Site-specific heterodimerization by paired class homeodomain proteins mediates selective transcriptional responses. J Biol Chem 274: 32325-32332
76. Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA 99: 4730-4735
77. Veraksa A, Del Campo M, McGinnis W (2000) Developmental patterning genes and their conserved functions: from model organisms to humans. Mol Genet Metab 69: 85-100
78. Vollbrecht E, Reiser L, Hake S (2000) Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knottedl. Development 127: 3161-3172
79. Williams-Carrier RE, Lie YS, Hake S, Lemaux PG (1997) Ectopic expression of the maize kn1 gene phenocopies the hooded mutant of barley. Development 124: 3737-3745
80. Wilson DS, Guenther B, Desplan C, Kuriyan J (1995) High resolution crystal structure of a paired (Pax) class cooperative homeodomain dimer on DNA. Cell 82: 709-719
81. Windhövel A, Hein I, Dabrowa R, Stockhaus J (2001) Characterization of a novel class of plant homeodomain proteins that bind to the C4 phosphoenolpyruvate carboxylase gene of Flaveria trinervia. Plant Mol Biol 45: 201-214
82. Wolberger C (1996) Homeodomain interactions. Curr Opin Struct Biol 6: 62-68
83. Wolberger C, Vershon AK, Liu B, Johnson AD, Pabo CO (1991) Crystal structure of a MAT alpha 2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67: 517-528
84. Wu X, Dabi T, Weigel D (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15: 436-440
85. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632