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Plant Molecular Biology

, 62:825 | Cite as

BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways

  • Nayelli Marsch-Martinez
  • Raffaella Greco
  • Jörg D. Becker
  • Shital Dixit
  • Jan H. W. Bergervoet
  • Aarati Karaba
  • Stefan de Folter
  • Andy Pereira
Article

Abstract

The BOLITA (BOL) gene, an AP2/ERF transcription factor, was characterized with the help of an activation tag mutant and overexpression lines in Arabidopsis and tobacco. The leaf size of plants overexpressing BOL was smaller than wild type plants due to a reduction in both cell size and cell number. Moreover, severe overexpressors showed ectopic callus formation in roots. Accordingly, global gene expression analysis using the overexpression mutant reflected the alterations in cell proliferation, differentiation and growth through expression changes in RBR, CYCD, and TCP genes, as well as genes involved in cell expansion (i.e. expansins and the actin remodeling factor ADF5). Furthermore, the expression of hormone signaling (i.e. auxin and cytokinin), biosynthesis (i.e. ethylene and jasmonic acid) and regulatory genes was found to be perturbed in bol-D mutant leaves.

Keywords

AP2/ERF transcription factor Organ size Cell growth Cell proliferation and differentiation Cell cycle CyclinD/retinoblastoma pathway 

Abbreviations

BL22-23

Brassinolide22-23

EBR

24-Epibrassinolide

BAP

Benzyl-amino-purine

NAA

Naphthalenacetic acid

IAA

Indole-3-acetic acid

ACC

1-Aminocyclopropane-1-carboxylic acid

AVG

Aminoethoxyvinylglycine

STS

Silver thiosulphate

SAUR

Small auxin up-regulated RNAs

Notes

Acknowledgements

We thank Robert Sevenier, Sacco de Vries and Cathy Albracht, Kim Boutilier, Asaph Aharoni, and Gert van Arkel for useful suggestions, discussions and help with materials, and Jeroen Peters and Wim Dirkse for technical help with the flow cytometry experiment. We are grateful to Jose Feijo and Margarida Oliveira as organizers of the 2004 EMBO course on Development at Oeiras, Portugal, and Assaf Zemach for collaboration during the global gene expression analysis. Isabelle Bertin is thanked for technical assistance, and Daan Jaspers and Gerrit Stunnenberg for plant care. J.D.B. was supported by fellowship SFRH/BPD/3619/2000 from Fundacão para a Ciência e a Tecnologia. S.D. and A.K. were supported by fellowships from WOTRO-NWO.

Supplementary material

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References

  1. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120PubMedCrossRefGoogle Scholar
  2. Alabadi D, Gil J, Blazquez MA, Garcia-Martinez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057PubMedCrossRefGoogle Scholar
  3. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17:5484–5496PubMedCrossRefGoogle Scholar
  4. 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 301:653–657PubMedCrossRefGoogle Scholar
  5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  6. Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618PubMedCrossRefGoogle Scholar
  7. Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inze D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743PubMedCrossRefGoogle Scholar
  8. Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630PubMedCrossRefGoogle Scholar
  9. Berger S, Bell E, Mullet JE (1996) Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiol 111:525–531PubMedGoogle Scholar
  10. Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332PubMedCrossRefGoogle Scholar
  11. Cheng S-H, Willmann MR, Chen H-C, Sheen J (2002) Calcium signaling through protein kinases. The arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485PubMedCrossRefGoogle Scholar
  12. Choe S, Tanaka A, Noguchi T, Fujioka S, Takatsuto S, Ross AS, Tax FE, Yoshida S, Feldmann KA (2000) Lesions in the sterol Δ7 reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J 21:431–443PubMedCrossRefGoogle Scholar
  13. Clough SJ, Bent AF (1998) Floral dip: a simplified method forAgrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  14. Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222PubMedCrossRefGoogle Scholar
  15. de Folter S, Busscher J, Colombo L, Losa A, Angenent GC (2004) Transcript profiling of transcription factor genes during silique development in Arabidopsis. Plant Mol Biol 56:351–366PubMedCrossRefGoogle Scholar
  16. De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J 39:537–559PubMedCrossRefGoogle Scholar
  17. Desvoyes B, Ramirez-Parra E, Xie Q, Chua N-H, Gutierrez C (2006) Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol 140:67–80PubMedCrossRefGoogle Scholar
  18. Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264PubMedCrossRefGoogle Scholar
  19. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92PubMedCrossRefGoogle Scholar
  20. Dong C-H, Xia G-X, Hong Y, Ramachandran S, Kost B, Chua N-H (2001) ADF proteins are involved in the control of flowering and regulate F-Actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346PubMedCrossRefGoogle Scholar
  21. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419PubMedCrossRefGoogle Scholar
  22. Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429:776–780Google Scholar
  23. Engelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res 4:288–290PubMedCrossRefGoogle Scholar
  24. Fleming AJ (2006) The co-ordination of cell division, differentiation and morphogenesis in the shoot apical meristem: a perspective. J Exp Bot 57:25–32PubMedCrossRefGoogle Scholar
  25. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404PubMedCrossRefGoogle Scholar
  26. Gallaher SR (1992) GUS protocols: using the GUS gene as a reporter of gene expression. Academic Press, INCGoogle Scholar
  27. Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JAH, Coen E, Doonan JH (2000) The expression of D-Cyclin genes defines distinct developmental zones in Snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148PubMedCrossRefGoogle Scholar
  28. Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523PubMedCrossRefGoogle Scholar
  29. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385PubMedCrossRefGoogle Scholar
  30. Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JAD, Peacock WJ, Dennis ES (1998) Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. PNAS 95:9019–9024PubMedCrossRefGoogle Scholar
  31. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1129–1231Google Scholar
  32. Hu Y, Xie Q, Chua N-H (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961PubMedCrossRefGoogle Scholar
  33. Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutierrez C, Doonan JH, Murray JAH (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37:155–169PubMedCrossRefGoogle Scholar
  34. Hwang I, Chen H-C, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515PubMedCrossRefGoogle Scholar
  35. Kiba T, Yamada H, Sato S, Kato T, Tabata S, Yamashino T, Mizuno T (2003) The Type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant Cell Physiol 44:868–874CrossRefGoogle Scholar
  36. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441PubMedCrossRefGoogle Scholar
  37. Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120PubMedCrossRefGoogle Scholar
  38. Kirch T, Simon R, Grunewald M, Werr W (2003) The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 Gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 15:694–705PubMedCrossRefGoogle Scholar
  39. Klahre U, Noguchi T, Fujioka S, Takatsuto S, Yokota T, Nomura T, Yoshida S, Chua N-H (1998) The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10:1677–1690PubMedCrossRefGoogle Scholar
  40. Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? . Curr Opin Plant Biol 3:488–492PubMedCrossRefGoogle Scholar
  41. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348PubMedCrossRefGoogle Scholar
  42. Kosugi S, Ohashi Y (2003) Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol 132:2012–2022PubMedCrossRefGoogle Scholar
  43. Kuhlemeier C, Reinhardt D (2001) Auxin and phyllotaxis. Trends Plant Sci 6:187–189PubMedCrossRefGoogle Scholar
  44. Kumaran MK, Bowman JL, Sundaresan V (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14:2761–2770PubMedCrossRefGoogle Scholar
  45. Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684PubMedCrossRefGoogle Scholar
  46. Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194PubMedCrossRefGoogle Scholar
  47. Leibfried A, To JPC, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175Google Scholar
  48. Liu Y-G, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674–681PubMedCrossRefGoogle Scholar
  49. Li C, Wong WH (2001a) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2:r0032.0031–r0032.0011Google Scholar
  50. Li C, Wong WH (2001b) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. PNAS 98:31–36CrossRefGoogle Scholar
  51. Li Y, Jones L, McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6:603–610PubMedCrossRefGoogle Scholar
  52. Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. PNAS 102:12978–12983PubMedCrossRefGoogle Scholar
  53. Magnani E, Sjolander K, Hake S (2004) From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 16:2265–2277PubMedCrossRefGoogle Scholar
  54. Marsch-Martinez N, Greco R, Van Arkel G, Herrera-Estrella L, Pereira A (2002) Activation tagging using the En-I maize␣transposon system in Arabidopsis. Plant Physiol 129:1544–1556PubMedCrossRefGoogle Scholar
  55. Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49PubMedCrossRefGoogle Scholar
  56. Menges M, de Jager SM, Gruissem W, Murray JAH (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566PubMedCrossRefGoogle Scholar
  57. Menges M, Samland AK, Planchais S, Murray JAH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906PubMedCrossRefGoogle Scholar
  58. Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539PubMedCrossRefGoogle Scholar
  59. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. PNAS 97:942–947PubMedCrossRefGoogle Scholar
  60. Mlynarova L, Loonen A, Heldens J, Jansen RC, Keizer P, Stiekema WJ, Nap JP (1994) Reduced position effect in mature transgenic plants conferred by the chicken lysozyme matrix-associated region. Plant Cell 6:417–426PubMedCrossRefGoogle Scholar
  61. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432PubMedCrossRefGoogle Scholar
  62. Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407PubMedCrossRefGoogle Scholar
  63. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. PNAS 94:7076–7081PubMedCrossRefGoogle Scholar
  64. Osakabe Y, Miyate S, Urao T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2002) Overexpression of Arabidopsis response␣regulators, ARR4/ATRR1/IBC7 and ARR8/ATRR3, alters cytokinin responses differentially in the shoot and in callus formation. Biochem Biophys Res Commun 293:806–815PubMedCrossRefGoogle Scholar
  65. Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841PubMedCrossRefGoogle Scholar
  66. Palatnik J, Allen E, Wu X, Schommer C, Schwab R, Carrington J, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  67. Ramirez-Parra E, Desvoyes B, Gutierrez C (2005) Balance between cell division and differentiation during plant development. Int J Dev Biol 49:467–477PubMedCrossRefGoogle Scholar
  68. Riechmann J, Meyerowitz E (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedCrossRefGoogle Scholar
  69. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110PubMedCrossRefGoogle Scholar
  70. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544PubMedCrossRefGoogle Scholar
  71. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009PubMedCrossRefGoogle Scholar
  72. Scherer GF (2002) Secondary messengers and phospholipase A2 in auxin signal transduction. Plant Mol Biol 49:357–372PubMedCrossRefGoogle Scholar
  73. Schrick K, Fujioka S, Takatsuto S, Stierhof Y-D, Stransky H, Yoshida S, Jurgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243PubMedCrossRefGoogle Scholar
  74. Siegfried K, Eshed Y, Baum S, Otsuga D, Drews G, Bowman J (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128PubMedGoogle Scholar
  75. Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6:63–73PubMedCrossRefGoogle Scholar
  76. Speulman E, Metz PLJ, van Arkel G, te Lintel Hekkert B, Stiekema WJ, Pereira A (1999) A two-component enhancer-inhibitor transposon mutagenesis system for functional analysis of the Arabidopsis genome. Plant Cell 11:1853–1866PubMedCrossRefGoogle Scholar
  77. Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553PubMedCrossRefGoogle Scholar
  78. Timpte CS, Wilson AK, Estelle M (1992) Effects of the axr2 mutation of Arabidopsis on cell shape in hypocotyl and inflorescence. Planta 188:271–278CrossRefGoogle Scholar
  79. Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894PubMedCrossRefGoogle Scholar
  80. To JPC, Haberer G, Ferreira FJ, Deruere J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16:658–671PubMedCrossRefGoogle Scholar
  81. Tsugeki R, Kochieva EZ, Fedoroff N (1996) A transposon insertion in the Arabidopsis SSR16 gene causes an embryo-defective lethal mutation. Plant J 10:479–489PubMedCrossRefGoogle Scholar
  82. Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49:547–555PubMedCrossRefGoogle Scholar
  83. van der Graaff E, Dulk-Ras A, Hooykaas P, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980PubMedGoogle Scholar
  84. Van Zhong G, Burns JK (2003) Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53:117–131PubMedCrossRefGoogle Scholar
  85. Verwoerd TC, Dekker BM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17:2362PubMedGoogle Scholar
  86. Vogler H, Kuhlemeier C (2003) Simple hormones but complex signalling. Curr Opin Plant Biol 6:51–56PubMedCrossRefGoogle Scholar
  87. Ward JM, Smith AM, Shah PK, Galanti SE, Yi H, Demianski AJ, van der Graaff E, Keller B, Neff MM (2006) A new role for the Arabidopsis AP2 transcription factor, LEAFY PETIOLE, in gibberellin-induced germination is revealed by the misexpression of a homologous gene, SOB2/DRN-LIKE. Plant Cell 18:29–39PubMedCrossRefGoogle Scholar
  88. Wasteneys G, Fujita M (2006) Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J␣Plant Res 119:5–10PubMedCrossRefGoogle Scholar
  89. Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100PubMedCrossRefGoogle Scholar
  90. Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349PubMedCrossRefGoogle Scholar
  91. Wilson K, Long D, Swinburne J, Coupland G (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671PubMedCrossRefGoogle Scholar
  92. Zhong S, Li C, Wong W (2003) ChipInfo: software for extracting gene annotation and gene ontology information for microarray analysis. Nucleic Acids Res 31:3483–3486PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Nayelli Marsch-Martinez
    • 1
  • Raffaella Greco
    • 1
  • Jörg D. Becker
    • 3
  • Shital Dixit
    • 1
  • Jan H. W. Bergervoet
    • 1
  • Aarati Karaba
    • 1
  • Stefan de Folter
    • 1
  • Andy Pereira
    • 2
  1. 1.Plant Research InternationalWageningen University and Research CentreWageningenThe Netherlands
  2. 2.Virginia Bioinformatics InstituteBlacksburgUSA
  3. 3.Centro de Biologia do DesenvolvimientoInstituto Gulbenkian de CiênciaOeirasPortugal

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