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On the genetic control of planar growth during tissue morphogenesis in plants

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Abstract

Tissue morphogenesis requires extensive intercellular communication. Plant organs are composites of distinct radial cell layers. A typical layer, such as the epidermis, is propagated by stereotypic anticlinal cell divisions. It is presently unclear what mechanisms coordinate cell divisions relative to the plane of a layer, resulting in planar growth and maintenance of the layer structure. Failure in the regulation of coordinated growth across a tissue may result in spatially restricted abnormal growth and the formation of a tumor-like protrusion. Therefore, one way to approach planar growth control is to look for genetic mutants that exhibit localized tumor-like outgrowths. Interestingly, plants appear to have evolved quite robust genetic mechanisms that govern these aspects of tissue morphogenesis. Here we provide a short summary of the current knowledge about the genetics of tumor formation in plants and relate it to the known control of coordinated cell behavior within a tissue layer. We further portray the integuments of Arabidopsis thaliana as an excellent model system to study the regulation of planar growth. The value of examining this process in integuments was established by the recent identification of the Arabidopsis AGC VIII kinase UNICORN as a novel growth suppressor involved in the regulation of planar growth and the inhibition of localized ectopic growth in integuments and other floral organs. An emerging insight is that misregulation of central determinants of adaxial–abaxial tissue polarity can lead to the formation of spatially restricted multicellular outgrowths in several tissues. Thus, there may exist a link between the mechanisms regulating adaxial–abaxial tissue polarity and planar growth in plants.

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References

  • Abrash EB, Bergmann DC (2009) Asymmetric cell divisions: a view from plant development. Dev Cell 16:783–796. doi:10.1016/j.devcel.2009.05.014

    Article  PubMed  CAS  Google Scholar 

  • Ahuja MR (1965) Genetic control of tumor formation in higher plants. Q Rev Biol 40:329–340

    Article  Google Scholar 

  • Ahuja MR (1998) Genetic tumors in Nicotiana and other plants. Q Rev Biol 73:439–462

    Article  Google Scholar 

  • Anthony RG, Henriques R, Helfer A, Mészáros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581. doi:10.1038/sj.emboj.7600068

    Article  PubMed  CAS  Google Scholar 

  • Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644. doi:10.1111/j.1365-313X.2008.03715.x

    Article  PubMed  CAS  Google Scholar 

  • Balasubramanian S, Schneitz K (2000) NOZZLE regulates proximal–distal pattern formation, cell proliferation and early sporogenesis in Arabidopsis thaliana. Development 127:4227–4238

    PubMed  CAS  Google Scholar 

  • Balasubramanian S, Schneitz K (2002) NOZZLE links proximal–distal and adaxial–abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129:4291–4300

    PubMed  CAS  Google Scholar 

  • Barbez E, Kubes M, Rolcik J, Beziat C, Pencik A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zazimalova E, Petrasek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485:119–122. doi:10.1038/nature11001

    Article  PubMed  CAS  Google Scholar 

  • Baud S, Bellec Y, Miquel M, Bellini C, Caboche M, Lepiniec L, Faure J-D, Rochat C (2004) Gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. EMBO Rep 5:515–520. doi:10.1038/sj.embor.7400124

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Stinard PS, McCarty DR (1996) CRINCLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Kang SH, Suh SG (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol 127:486–496

    Article  PubMed  CAS  Google Scholar 

  • Beemster GTS, Fiorani F, Inzé D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158

    Article  PubMed  CAS  Google Scholar 

  • Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser M-T, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70

    PubMed  CAS  Google Scholar 

  • Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067

    PubMed  CAS  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  CAS  Google Scholar 

  • Berger AH, Knudson AG, Pandolfi PP (2011) A continuum model for tumour suppression. Nature 476:163–169. doi:10.1038/nature10275

    Article  PubMed  CAS  Google Scholar 

  • Besson S, Dumais J (2011) Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci U S A 108:6294–6299. doi:10.1073/pnas.1011866108

    Article  PubMed  CAS  Google Scholar 

  • Blakeslee AF, Satina S (1947) Ovular tumors associated with hybrid embryos in Datura. Science 105:633

    PubMed  CAS  Google Scholar 

  • Bögre L, Ökrész L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8:424–431

    Article  PubMed  CAS  Google Scholar 

  • Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445. doi:10.1146/annurev-phyto-080508-081923

    Article  PubMed  CAS  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmuller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7:e1002051. doi:10.1371/journal.ppat.1002051

    Article  PubMed  CAS  Google Scholar 

  • Carpten JD, Faber AL, Horn C, Donoho GP, Briggs SL, Robbins CM, Hostetter G, Boguslawski S, Moses TY, Savage S, Uhlik M, Lin A, Du J, Qian YW, Zeckner DJ, Tucker-Kellogg G, Touchman J, Patel K, Mousses S, Bittner M, Schevitz R, Lai MH, Blanchard KL, Thomas JE (2007) A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature 448:439–444. doi:10.1038/nature05933

    Article  PubMed  CAS  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131:5263–5276. doi:10.1242/dev.01400

    Article  PubMed  CAS  Google Scholar 

  • Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226:1183–1194. doi:10.1007/s00425-007-0565-4

    Article  PubMed  CAS  Google Scholar 

  • Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100:469–478

    Article  PubMed  CAS  Google Scholar 

  • Colombo L, Battaglia R, Kater MM (2008) Arabidopsis ovule development and its evolutionary conservation. Trends Plant Sci 13:444–450. doi:10.1016/j.tplants.2008.04.011

    Article  PubMed  CAS  Google Scholar 

  • Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97:3718–3723

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Beeckman T (2011) Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat Rev Mol Cell Biol 12:177–188. doi:10.1038/nrm3064

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jurgens G, Ingram GC, Inze D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597. doi:10.1126/science.1160158

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P (2011) PIN polarity regulation by AGC-3 kinases and ARF-GEF: a recurrent theme with context dependent modifications for plant development and response. Plant Signal Behav 6:1333–1337

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P, Mathur J, Hülskamp M, Gadella TWJ (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3:11. doi:10.1186/1741-7007-3-11

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P, Weits DA, Cruz-Ramirez A, Deinum EE, Tindemans SH, Kakar K, Prasad K, Mahonen AP, Ambrose C, Sasabe M, Wachsmann G, Luijten M, Bennett T, Machida Y, Heidstra R, Wasteneys G, Mulder BM, Scheres B (2012) A PLETHORA-auxin transcription module controls cell division plane rotation through MAP65 and CLASP. Cell 149:383–396. doi:10.1016/j.cell.2012.02.051

    Article  PubMed  CAS  Google Scholar 

  • Dodueva IE, Frolova NV, Lutova LA (2007) Plant tumorigenesis: different ways for shifting systemic control of plant cell division and differentiation. Transgen Plant J 1:17–38

    Google Scholar 

  • Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kuhnemann J, Sonnewald U, Kahmann R, Kamper J (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195. doi:10.1111/j.1365-313X.2008.03590.x

    Article  PubMed  CAS  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84

    PubMed  CAS  Google Scholar 

  • Doonan JH, Sablowski R (2010) Walls around tumours—why plants do not develop cancer. Nat Rev Cancer 10:794–802. doi:10.1038/nrc2942

    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

    Article  PubMed  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    PubMed  CAS  Google Scholar 

  • 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 KANADI genes. Curr Biol 13:1768–1774

    Article  PubMed  CAS  Google Scholar 

  • Enugutti B, Kirchhelle C, Oelschner M, Schliebner I, Leister D, Schneitz K (2012) Regulation of planar growth by the Arabidopsis AGC protein kinase UNICORN. Proc Natl Acad Sci USA 109:15060–15065. doi:10.1073/pnas.1205089109

    Google Scholar 

  • Eshed Y, Baum SF, Perea JV, Bowman J (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006. doi:10.1242/dev.01186

    Article  PubMed  CAS  Google Scholar 

  • Faure J-D, Vittorioso P, Santoni V, Fraisier V, Prinsen E, Barlier I, Van Onckelen H, Caboche M, Bellini C (1998) The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development 125:909–918

    PubMed  CAS  Google Scholar 

  • Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, Palme K, Scheres B, Grebe M (2006) Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity. Curr Biol 16:2143–2149. doi:10.1016/j.cub.2006.08.091

    Article  PubMed  CAS  Google Scholar 

  • Frank M, Guivarc'h A, Krupkova E, Lorenz-Meyer I, Chriqui D, Schmülling T (2002) TUMOROUS SHOOT DEVELOPMENT (TSD) genes are required for co-ordinated plant shoot development. Plant J 29:73–85

    Article  PubMed  CAS  Google Scholar 

  • Galván-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci 12:541–547. doi:10.1016/j.tplants.2007.10.004

    Article  PubMed  CAS  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    Article  PubMed  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, Muller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194. doi:10.1111/j.1365-313X.2005.02519.x

    Article  PubMed  CAS  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the "gene-jockeying" tool. Microbiol Mol Biol Rev 67:16–37. doi:10.1128/MMBR.67.1.16-37.2003

    Article  PubMed  CAS  Google Scholar 

  • Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130:4249–4258

    Article  PubMed  CAS  Google Scholar 

  • Grebe M (2004) Ups and downs of tissue and planar polarity in plants. Bioessays 26:719–729. doi:10.1002/bies.20065

    Article  PubMed  CAS  Google Scholar 

  • Grebe M (2010) Cell polarity: lateral perspectives. Curr Biol 20:R446–R448. doi:10.1016/j.cub.2010.03.035

    Article  PubMed  CAS  Google Scholar 

  • Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M, Palme K, Bennett MJ, Scheres B (2002) Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr Biol 12:329–334

    Article  PubMed  CAS  Google Scholar 

  • Gunning BES, Hughes JE, Hardham AR (1978) Formative and proliferative cell divisions, cell differentiation, and developmental changes in the meristem of Azolla roots. Planta 143:121–144

    Article  Google Scholar 

  • Haber D, Harlow E (1997) Tumour-suppressor genes: evolving definitions in the genomic age. Nat Genet 16:320–322. doi:10.1038/ng0897-320

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Erschadi S, Torres-Ruiz RA (2002) The Arabidopsis gene PEPINO/PASTICCINO2 is required for proliferation control of meristematic and non-meristematic cells and encodes a putative anti-phosphatase. Dev Genes Evol 212:542–550

    Article  PubMed  CAS  Google Scholar 

  • Halder G, Johnson RL (2011) Hippo signaling: growth control and beyond. Development 138:9–22. doi:10.1242/dev.045500

    Article  PubMed  CAS  Google Scholar 

  • Harashima H, Schnittger A (2010) The integration of cell division, growth and differentiation. Curr Opin Plant Biol 13:66–74. doi:10.1016/j.pbi.2009.11.001

    Article  PubMed  CAS  Google Scholar 

  • Henriques R, Magyar Z, Monardes A, Khan S, Zalejski C, Orellana J, Szabados L, de la Torre C, Koncz C, Bögre L (2010) Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J 29:2979–2993. doi:10.1038/emboj.2010.164

    Article  PubMed  CAS  Google Scholar 

  • Hergovich A, Hemmings BA (2012) Hippo signalling in the G2/M cell cycle phase: lessons learned from the yeast MEN and SIN pathways. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2012.04.001

  • Hergovich A, Stegert MR, Schmitz D, Hemmings BA (2006) NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 7:253–264. doi:10.1038/nrm1891

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hunter CT, Kirienko DH, Sylvester AW, Peter GF, McCarty DR, Koch KE (2012) Cellulose Synthase-Like D1 is integral to normal cell division, expansion, and leaf development in maize. Plant Physiol 158:708–724. doi:10.1104/pp. 111.188466

    Article  PubMed  CAS  Google Scholar 

  • Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997. doi:10.1101/gad.1819909

    Article  PubMed  CAS  Google Scholar 

  • Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M (2009) Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 11:731–738. doi:10.1038/ncb1879

    Article  PubMed  CAS  Google Scholar 

  • Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, Ohme-Takagi M (2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514. doi:10.1016/j.cub.2011.02.020

    Article  PubMed  CAS  Google Scholar 

  • Izhaki A, Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19:495–508. doi:10.1105/tpc.106.047472

    Article  PubMed  CAS  Google Scholar 

  • Jenik PD, Irish VF (2000) Regulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development. Development 127:1267–1276

    PubMed  CAS  Google Scholar 

  • Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ (1995) The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev 9:534–546

    Article  PubMed  CAS  Google Scholar 

  • Kelley DR, Gasser CS (2009) Ovule development: genetic trends and evolutionary considerations. Sex Plant Reprod 22:229–234. doi:10.1007/s00497-009-0107-2

    Article  PubMed  Google Scholar 

  • Kelley DR, Skinner DJ, Gasser CS (2009) Roles of polarity determinants in ovule development. Plant J 57:1054–1064. doi:10.1111/j.1365-313X.2008.03752.x

    Article  PubMed  CAS  Google Scholar 

  • Kelley DR, Arreola A, Gallagher TL, Gasser CS (2012) ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis. Development 139(6):1105–1109. doi:10.1242/dev.067918

    Article  PubMed  CAS  Google Scholar 

  • Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709

    Article  PubMed  CAS  Google Scholar 

  • Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153. doi:10.1105/tpc.8.2.137

    PubMed  CAS  Google Scholar 

  • Kostoff D (1939) Abnormal mitosis in tobacco plants forming hereditary tumor. Nature 144:599

    Article  Google Scholar 

  • Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249. doi:10.1186/gb-2009-10-12-249

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA (2003) AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain. Nucleic Acids Res 31:1859–1868

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. The Plant Cell 12:1357–1366

    PubMed  CAS  Google Scholar 

  • Krupkova E, Schmülling T (2009) Developmental consequences of the tumorous shoot development1 mutation, a novel allele of the cellulose-synthesizing KORRIGAN1 gene. Plant Mol Biol 71:641–655. doi:10.1007/s11103-009-9546-2

    Article  PubMed  CAS  Google Scholar 

  • Krupkova E, Immerzeel P, Pauly M, Schmülling T (2007) The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J 50:735–750. doi:10.1111/j.1365-313X.2007.03123.x

    Article  PubMed  CAS  Google Scholar 

  • Léon-Kloosterziel KM, Keijzer CJ, Koornneef M (1994) A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6:385–392

    PubMed  Google Scholar 

  • Liu Z, Franks RG, Klink VP (2000) Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12:1879–1892

    PubMed  CAS  Google Scholar 

  • Long J, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 218:341–353

    Article  PubMed  CAS  Google Scholar 

  • Martin FW (1966) Frosty spot. A developmental disturbance of the tomato leaf. Ann Bot 30:701–709

    Google Scholar 

  • Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:1335–1346

    PubMed  CAS  Google Scholar 

  • McAbee JM, Hill TA, Skinner DJ, Izhaki A, Hauser BA, Meister RJ, Venugopala Reddy G, Meyerowitz EM, Bowman JL, Gasser CS (2006) ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. Plant J 46:522–531

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci U S A 97:942–947. doi:10.1073/pnas.97.2.942

    Article  PubMed  CAS  Google Scholar 

  • Motose H, Tominaga R, Wada T, Sugiyama M, Watanabe Y (2008) A NIMA-related protein kinase suppresses ectopic outgrowth of epidermal cells through its kinase activity and the association with microtubules. Plant J 54:829–844. doi:10.1111/j.1365-313X.2008.03445.x

    Article  PubMed  CAS  Google Scholar 

  • Mouille G, Ralet MC, Cavelier C, Eland C, Effroy D, Hematy K, McCartney L, Truong HN, Gaudon V, Thibault JF, Marchant A, Höfte H (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J 50:605–614. doi:10.1111/j.1365-313X.2007.03086.x

    Article  PubMed  CAS  Google Scholar 

  • Müller S, Wright AJ, Smith LG (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19:180–188. doi:10.1016/j.tcb.2009.02.002

    Article  PubMed  CAS  Google Scholar 

  • Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10:e1001299. doi:10.1371/journal.pbio.1001299

    Article  PubMed  CAS  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Hofte H (1998) A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576. doi:10.1093/emboj/17.19.5563

    Article  PubMed  CAS  Google Scholar 

  • Nole-Wilson S, Krizek BA (2000) DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA. Nucleic Acids Resesarch 28:4076–4082

    Article  CAS  Google Scholar 

  • Nuttall VW, Lyall LH (1964) Inheritance of neoplastic pod in the pea. J Hered 55:184–186

    Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science. doi:10.1126/science.1167324

  • Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11:9–22. doi:10.1038/nrm2822

    Article  PubMed  CAS  Google Scholar 

  • Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  PubMed  CAS  Google Scholar 

  • Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408. doi:10.1016/j.tplants.2009.05.002

    Article  PubMed  CAS  Google Scholar 

  • Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446. doi:10.1101/cshperspect.a001446

    Article  PubMed  CAS  Google Scholar 

  • Petricka JJ, Van Norman JM, Benfey PN (2009) Symmetry breaking in plants: molecular mechanisms regulating asymmetric cell divisions in Arabidopsis. Cold Spring Harb Perspect Biol 1:a000497. doi:10.1101/cshperspect.a000497

    Article  PubMed  Google Scholar 

  • Pickett-Heaps JD, Northcote DH (1966) Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci 1:109–120

    PubMed  CAS  Google Scholar 

  • Pietra S, Grebe M (2010) Auxin paves the way for planar morphogenesis. Cell 143:29–31. doi:10.1016/j.cell.2010.09.029

    Article  PubMed  CAS  Google Scholar 

  • Pinon V, Etchells JP, Rossignol P, Collier SA, Arroyo JM, Martienssen RA, Byrne ME (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135:1315–1324. doi:10.1242/dev.016469

    Article  PubMed  CAS  Google Scholar 

  • Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29:1021–1032. doi:10.1038/emboj.2010.8

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen CG, Humphries JA, Smith LG (2011) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62:387–409. doi:10.1146/annurev-arplant-042110-103802

    Article  PubMed  CAS  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861. doi:10.1038/nature02353

    Article  PubMed  CAS  Google Scholar 

  • Reynolds JO, Eisses JF, Sylvester AW (1998) Balancing division and expansion during maize leaf morphogenesis: analysis of the mutant, warty-1. Development 125:259–268

    PubMed  CAS  Google Scholar 

  • Robinson-Beers K, Pruitt RE, Gasser CS (1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4:1237–1249. doi:10.1105/tpc.4.10.1237

    PubMed  Google Scholar 

  • Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394. doi:10.1146/annurev.phyto.43.040204.135939

    Article  PubMed  CAS  Google Scholar 

  • Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui JC, Bellec Y, Renne C, Miquel M, Dacosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure JD (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375. doi:10.1105/tpc.109.071209

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfeldt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Satina S, Blakeslee AF, Avery AG (1940) Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. Am J Bot 27:895–905

    Article  Google Scholar 

  • Schatlowski N, Stahl Y, Hohenstatt ML, Goodrich J, Schubert D (2010) The CURLY LEAF interacting protein BLISTER controls expression of polycomb-group target genes and cellular differentiation of Arabidopsis thaliana. Plant Cell 22:2291–2305. doi:10.1105/tpc.109.073403

    Article  PubMed  CAS  Google Scholar 

  • Schneitz K, Hülskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749. doi:10.1046/j.1365-313X.1995.07050731.x

    Article  Google Scholar 

  • Schneitz K, Hülskamp M, Kopczak SD, Pruitt RE (1997) Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 124:1367–1376

    PubMed  CAS  Google Scholar 

  • Schneitz K, Baker SC, Gasser CS, Redweik A (1998) Pattern formation and growth during floral organogenesis: HUELLENLOS and AINTEGUMENTA are required for the formation of the proximal region of the ovule primordium in Arabidopsis thaliana. Development 125:2555–2563

    PubMed  CAS  Google Scholar 

  • Sharp WR, Gunckel JE (1969) Physiological comparisons of pith callus with crown-gall and genetic tumors of Nicotiana glauca, N. langsdorffii, and N. glauca-langsdorffii grown in vitro. I. Tumor induction and proliferation. Plant Physiol 44:1069–1072

    Article  PubMed  CAS  Google Scholar 

  • Sherr CJ (2004) Principles of tumor suppression. Cell 116:235–246

    Article  PubMed  CAS  Google Scholar 

  • Sieber P, Gheyeselinck J, Gross-Hardt R, Laux T, Grossniklaus U, Schneitz K (2004) Pattern formation during early ovule development in Arabidopsis thaliana. Dev Biol 273:321–334

    Article  PubMed  CAS  Google Scholar 

  • Sieberer T, Hauser M-T, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842. doi:10.1016/S0960-9822(03)00327-0

    Article  PubMed  CAS  Google Scholar 

  • Skibbe DS, Doehlemann G, Fernandes J, Walbot V (2010) Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89–92. doi:10.1126/science.1185775

    Article  PubMed  CAS  Google Scholar 

  • Skinner D, Gasser C (2009) Expression-based discovery of candidate ovule development regulators through transcriptional profiling of ovule mutants. BMC Plant Biol 9:29. doi:10.1186/1471-2229-9-29

    Article  PubMed  CAS  Google Scholar 

  • Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 54:118–130

    Google Scholar 

  • Smith LM, Bomblies K, Weigel D (2011) Complex evolutionary events at a tandem cluster of Arabidopsis thaliana genes resulting in a single-locus genetic incompatibility. PLoS Genet 7:e1002164. doi:10.1371/journal.pgen.1002164

    Article  PubMed  CAS  Google Scholar 

  • St John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow AF, McGrath J, Xu T (1999) Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet 21:182–186. doi:10.1038/5965

    Article  PubMed  CAS  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914. doi:10.1016/j.cub.2009.03.060

    Article  PubMed  CAS  Google Scholar 

  • Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. doi:10.1016/j.devcel.2010.02.004

    Article  PubMed  CAS  Google Scholar 

  • Szakonyi D, Moschopoulos A, Byrne ME (2010) Perspectives on leaf dorsoventral polarity. J Plant Res 123:281–290. doi:10.1007/s10265-010-0336-3

    Article  PubMed  Google Scholar 

  • Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, Tsukaya H, Ikezaki M, Machida C, Machida Y (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134:1643–1652

    Article  PubMed  CAS  Google Scholar 

  • Tilney-Bassett RAE (1986) Plant chimeras. Edward Arnold, London

    Google Scholar 

  • Torres-Ruiz RA, Lohner A, Jürgens G (1996) The GURKE gene is required for normal organisation of the apical region in the Arabidopsis embryo. Plant J 10:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Truernit E, Haseloff J (2008) Arabidopsis thaliana outer ovule integument morphogenesis: ectopic expression of KNAT1 reveals a compensation mechanism. BMC Plant Biol 8:35. doi:10.1186/1471-2229-8-35

    Article  PubMed  CAS  Google Scholar 

  • Valvekens D, Van Montagu M, Lijsebettens M (1988) Agrobacterium tumefaciens mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85:5536–5540

    Article  PubMed  CAS  Google Scholar 

  • Vivanco I, Sawyers CL (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2:489–501. doi:10.1038/nrc839

    Article  PubMed  CAS  Google Scholar 

  • Wachsman G, Heidstra R, Scheres B (2011) Distinct cell-autonomous functions of RETINOBLASTOMA-RELATED in Arabidopsis stem cells revealed by the brother of brainbow clonal analysis system. Plant Cell 23:2581–2591. doi:10.1105/tpc.111.086199

    Article  PubMed  CAS  Google Scholar 

  • Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154

    CAS  Google Scholar 

  • Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308

    Article  PubMed  CAS  Google Scholar 

  • Weinberg RA (2006) The biology of cancer. Garland Science, New York

    Google Scholar 

  • Xu T, Wang W, Zhang S, Stewart RA, Yu W (1995) Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121:1053–1063

    PubMed  CAS  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110. doi:10.1016/j.cell.2010.09.003

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, McCormick S (2009) AGCVIII kinases: at the crossroads of cellular signaling. Trends Plant Sci 14:689–695. doi:10.1016/j.tplants.2009.09.006

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, He J, McCormick S (2009) Two Arabidopsis AGC kinases are critical for the polarized growth of pollen tubes. Plant J 58:474–484. doi:10.1111/j.1365-313X.2009.03792.x

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Work on planar growth in the laboratory of the authors is supported by grants from the Deutsche Forschungsgemeinschaft (DFG).

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The authors declare that they have no conflict of interest.

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Enugutti, B., Kirchhelle, C. & Schneitz, K. On the genetic control of planar growth during tissue morphogenesis in plants. Protoplasma 250, 651–661 (2013). https://doi.org/10.1007/s00709-012-0452-0

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