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

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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.

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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

References

  • 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 119:109–120

    Article  PubMed  CAS  Google Scholar 

  • Alabadi D, Gil J, Blazquez MA, Garcia-Martinez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057

    Article  PubMed  CAS  Google Scholar 

  • 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 17:5484–5496

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

    Article  PubMed  CAS  Google Scholar 

  • 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 138:734–743

    Article  PubMed  CAS  Google Scholar 

  • Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630

    Article  PubMed  CAS  Google Scholar 

  • 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 111:525–531

    PubMed  CAS  Google Scholar 

  • 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 29:325–332

    Article  PubMed  CAS  Google Scholar 

  • 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 129:469–485

    Article  PubMed  CAS  Google Scholar 

  • 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 21:431–443

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method forAgrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  PubMed  CAS  Google Scholar 

  • 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 56:351–366

    Article  PubMed  CAS  Google Scholar 

  • 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 39:537–559

    Article  PubMed  CAS  Google Scholar 

  • 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 140:67–80

    Article  PubMed  CAS  Google Scholar 

  • Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264

    Article  PubMed  CAS  Google Scholar 

  • 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 15:79–92

    Article  PubMed  CAS  Google Scholar 

  • 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 13:1333–1346

    Article  PubMed  CAS  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419

    Article  PubMed  CAS  Google Scholar 

  • Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429:776–780

    Google Scholar 

  • Engelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res 4:288–290

    Article  PubMed  Google Scholar 

  • Fleming AJ (2006) The co-ordination of cell division, differentiation and morphogenesis in the shoot apical meristem: a perspective. J Exp Bot 57:25–32

    Article  PubMed  CAS  Google Scholar 

  • 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 12:393–404

    Article  PubMed  CAS  Google Scholar 

  • Gallaher SR (1992) GUS protocols: using the GUS gene as a reporter of gene expression. Academic Press, INC

  • 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 122:1137–1148

    Article  PubMed  CAS  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Article  PubMed  CAS  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  PubMed  CAS  Google Scholar 

  • 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 95:9019–9024

    Article  PubMed  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1129–1231

    Google Scholar 

  • Hu Y, Xie Q, Chua N-H (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961

    Article  PubMed  CAS  Google Scholar 

  • 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 37:155–169

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Chen H-C, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515

    Article  PubMed  CAS  Google Scholar 

  • 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 44:868–874

    Article  CAS  Google Scholar 

  • 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 72:427–441

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    Article  PubMed  CAS  Google Scholar 

  • 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 15:694–705

    Article  PubMed  CAS  Google Scholar 

  • 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 10:1677–1690

    Article  PubMed  CAS  Google Scholar 

  • Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? . Curr Opin Plant Biol 3:488–492

    Article  PubMed  CAS  Google Scholar 

  • Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348

    Article  PubMed  CAS  Google Scholar 

  • 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 132:2012–2022

    Article  PubMed  CAS  Google Scholar 

  • Kuhlemeier C, Reinhardt D (2001) Auxin and phyllotaxis. Trends Plant Sci 6:187–189

    Article  PubMed  CAS  Google Scholar 

  • Kumaran MK, Bowman JL, Sundaresan V (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14:2761–2770

    Article  PubMed  CAS  Google Scholar 

  • Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684

    Article  PubMed  CAS  Google Scholar 

  • Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194

    Article  PubMed  CAS  Google Scholar 

  • 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 438:1172–1175

    Google Scholar 

  • 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 25:674–681

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wong WH (2001a) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2:r0032.0031–r0032.0011

    Google Scholar 

  • Li C, Wong WH (2001b) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. PNAS 98:31–36

    Article  CAS  Google Scholar 

  • Li Y, Jones L, McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6:603–610

    Article  PubMed  CAS  Google Scholar 

  • Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. PNAS 102:12978–12983

    Article  PubMed  CAS  Google Scholar 

  • Magnani E, Sjolander K, Hake S (2004) From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 16:2265–2277

    Article  PubMed  CAS  Google Scholar 

  • 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 129:1544–1556

    Article  PubMed  CAS  Google Scholar 

  • Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49

    Article  PubMed  CAS  Google Scholar 

  • 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 41:546–566

    Article  PubMed  CAS  Google Scholar 

  • 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 18:893–906

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. PNAS 97:942–947

    Article  PubMed  CAS  Google Scholar 

  • 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 6:417–426

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  Google Scholar 

  • Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  PubMed  CAS  Google Scholar 

  • 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 94:7076–7081

    Article  PubMed  CAS  Google Scholar 

  • 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 293:806–815

    Article  PubMed  CAS  Google Scholar 

  • Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841

    Article  PubMed  CAS  Google Scholar 

  • Palatnik J, Allen E, Wu X, Schommer C, Schwab R, Carrington J, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  PubMed  CAS  Google Scholar 

  • Ramirez-Parra E, Desvoyes B, Gutierrez C (2005) Balance between cell division and differentiation during plant development. Int J Dev Biol 49:467–477

    Article  PubMed  Google Scholar 

  • Riechmann J, Meyerowitz E (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    Article  PubMed  CAS  Google Scholar 

  • 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 290:2105–2110

    Article  PubMed  CAS  Google Scholar 

  • Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544

    Article  PubMed  CAS  Google Scholar 

  • 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 290:998–1009

    Article  PubMed  CAS  Google Scholar 

  • Scherer GF (2002) Secondary messengers and phospholipase A2 in auxin signal transduction. Plant Mol Biol 49:357–372

    Article  PubMed  CAS  Google Scholar 

  • 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 38:227–243

    Article  PubMed  CAS  Google Scholar 

  • 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 126:4117–4128

    PubMed  CAS  Google Scholar 

  • Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6:63–73

    Article  PubMed  Google Scholar 

  • 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 11:1853–1866

    Article  PubMed  CAS  Google Scholar 

  • Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553

    Article  PubMed  CAS  Google Scholar 

  • Timpte CS, Wilson AK, Estelle M (1992) Effects of the axr2 mutation of Arabidopsis on cell shape in hypocotyl and inflorescence. Planta 188:271–278

    Article  CAS  Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  PubMed  CAS  Google Scholar 

  • 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 16:658–671

    Article  PubMed  CAS  Google Scholar 

  • Tsugeki R, Kochieva EZ, Fedoroff N (1996) A transposon insertion in the Arabidopsis SSR16 gene causes an embryo-defective lethal mutation. Plant J 10:479–489

    Article  PubMed  CAS  Google Scholar 

  • Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49:547–555

    Article  PubMed  Google Scholar 

  • 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 127:4971–4980

    PubMed  Google Scholar 

  • Van Zhong G, Burns JK (2003) Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53:117–131

    Article  PubMed  CAS  Google Scholar 

  • Verwoerd TC, Dekker BM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17:2362

    PubMed  CAS  Google Scholar 

  • Vogler H, Kuhlemeier C (2003) Simple hormones but complex signalling. Curr Opin Plant Biol 6:51–56

    Article  PubMed  CAS  Google Scholar 

  • 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 18:29–39

    Article  PubMed  CAS  Google Scholar 

  • Wasteneys G, Fujita M (2006) Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J␣Plant Res 119:5–10

    Article  PubMed  Google Scholar 

  • Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100

    Article  PubMed  CAS  Google Scholar 

  • 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 123:1337–1349

    Article  PubMed  CAS  Google Scholar 

  • 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 8:659–671

    Article  PubMed  CAS  Google Scholar 

  • Zhong S, Li C, Wong W (2003) ChipInfo: software for extracting gene annotation and gene ontology information for microarray analysis. Nucleic Acids Res 31:3483–3486

    Article  PubMed  CAS  Google Scholar 

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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.

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  1. Andy Pereira

    Present address: Virginia Bioinformatics Institute, Washington Street, Blacksburg, VA, 24061, USA

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  1. Plant Research International, Wageningen University and Research Centre, PO Box 16, 6700 AA, Wageningen, The Netherlands

    Nayelli Marsch-Martinez, Raffaella Greco, Shital Dixit, Jan H. W. Bergervoet, Aarati Karaba & Stefan de Folter

  2. Centro de Biologia do Desenvolvimiento, Instituto Gulbenkian de Ciência, 2780-156, Oeiras, Portugal

    Jörg D. Becker

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Nayelli Marsch-Martinez and Raffaella Greco contributed equally to this work.

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Marsch-Martinez, N., Greco, R., Becker, J.D. et al. BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62, 825–843 (2006). https://doi.org/10.1007/s11103-006-9059-1

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