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JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root

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Abstract

The plant hormone auxin plays a role in virtually every aspect of plant growth and development. Temporal and spatial distribution of auxin largely depends on the dynamic expression and subcellular localization of the PIN auxin-efflux carrier proteins. We show here that the Arabidopsis thaliana JAGGED LATERAL ORGAN (JLO) gene, a member of the LATERAL ORGAN BOUNDARY DOMAIN (LBD) gene family, is required for coordinated cell division during embryogenesis. JLO promotes expression of several PINFORMED (PIN) genes during embryonic and root development. Inducible JLO misexpression reveals that JLO activity is sufficient for rapid and high level PIN1 and PIN3 transcription. Genes of the PLETHORA (PLT) family respond to auxin and direct PIN expression, but PLT genes were severely underexpressed in jlo mutants. JLO controls embryonic patterning together with the auxin dependent MONOPTEROS/BODENLOS pathway, but is itself only mildly auxin inducible. We further show that all known auxin responses in the root require JLO activity. We thereby identify JLO as a central regulator of auxin distribution and signaling throughout plant development.

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References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176

    Article  CAS  PubMed  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808

    Article  CAS  PubMed  Google Scholar 

  • Bureau M, Simon R (2008) JLO regulates embryo patterning and organ initiation by controlling auxin transport. Plant Signal Behav 3:145–147

    PubMed  Google Scholar 

  • Chalfun-Junior A, Franken J, Mes JJ, Marsch-Martinez N, Pereira A, Angenent GC (2005) ASYMMETRIC LEAVES2-LIKE1 gene, a member of the AS2/LOB family, controls proximal-distal patterning in Arabidopsis petals. Plant Mol Biol 57:559–575

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    Article  CAS  PubMed  Google Scholar 

  • De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W, Naudts M, Levesque MP, Ehrismann JS, Inze D, Luschnig C, Benfey PN, Weijers D, Van Montagu MC, Bennett MJ, Jurgens G, Beeckman T (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci USA 107:2705–2710

    Article  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  CAS  PubMed  Google Scholar 

  • Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    PubMed  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  PubMed  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Galweiler L, Guan C, Muller 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  CAS  PubMed  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  CAS  PubMed  Google Scholar 

  • Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    Article  CAS  PubMed  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    Article  CAS  PubMed  Google Scholar 

  • Hejatko J, Blilou I, Brewer PB, Friml J, Scheres B, Benkova E (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat Protoc 1:1939–1946

    Article  CAS  PubMed  Google Scholar 

  • Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:1057–1070

    Article  CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2004) Auxin-induced SCFTIR1-Aux/IAA interaction involves stable modification of the SCFTIR1 complex. Proc Natl Acad Sci USA 101:12381–12386

    Article  CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24:447–473

    Article  CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Langowski L, Wisniewska J, Dhonukshe P, Brewer PB, Friml J (2008a) Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol Plant 1:1056–1066

    Article  CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J (2008b) Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA 105:17812–17817

    Article  CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J (2008c) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531

    Article  CAS  PubMed  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  PubMed  Google Scholar 

  • Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056

    Article  CAS  PubMed  Google Scholar 

  • Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1:a001545

    Article  PubMed  Google Scholar 

  • Muller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946

    Article  PubMed  Google Scholar 

  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130

    Article  CAS  PubMed  Google Scholar 

  • Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    Article  CAS  PubMed  Google Scholar 

  • Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177

    Article  CAS  PubMed  Google Scholar 

  • Ploense SE, Wu MF, Nagpal P, Reed JW (2009) A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning. Development 136:1509–1517

    Article  CAS  PubMed  Google Scholar 

  • Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425

    Article  CAS  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt 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  CAS  PubMed  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    Article  CAS  PubMed  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911

    Article  CAS  PubMed  Google Scholar 

  • Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    Article  CAS  PubMed  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453

    Article  CAS  PubMed  Google Scholar 

  • Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761

    Article  CAS  PubMed  Google Scholar 

  • Soyano T, Thitamadee S, Machida Y, Chua NH (2008) ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 20:3359–3373

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543

    Article  CAS  PubMed  Google Scholar 

  • Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, Palauqui JC (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20:1494–1503

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed  Google Scholar 

  • Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531

    Article  CAS  PubMed  Google Scholar 

  • Weijers D, Jurgens G (2005) Auxin and embryo axis formation: the ends in sight? Curr Opin Plant Biol 8:32–37

    Article  CAS  PubMed  Google Scholar 

  • Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885

    Article  CAS  PubMed  Google Scholar 

  • Zazimalova E, Krecek P, Skupa P, Hoyerova K, Petrasek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Carin Theres and Cornelia Gieseler for technical support and to members of the R.S. laboratory for critical comments. We specifically thank Jiri Friml, Frans Tax, Thomas Berleth, Gerd Jürgens, Dolf Weijers and Ben Scheres for generously supplying plant materials. This work was funded through an EU Marie Curie Research and Training Network “SyStem”, grant number MCRTN-CT-2004005336, and the DFG through grants Si677/2-1, 2-2 and Si947/3-1.

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  1. Institut für Genetik, Heinrich-Heine-Universität, Universitätstr. 1, 40225, Düsseldorf, Germany

    Marina Bureau, Madlen I. Rast, Jasmin Illmer & Rüdiger Simon

  2. Institut de Biologie Moléculaire des Plantes UPR-CNRS2357, 12 rue du Général Zimmer, 67084, Strasbourg Cedex, France

    Marina Bureau

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  1. Marina Bureau
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  2. Madlen I. Rast
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Correspondence to Rüdiger Simon.

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Marina Bureau, Madlen I. Rast contributed equally to this work.

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Bureau, M., Rast, M.I., Illmer, J. et al. JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Mol Biol 74, 479–491 (2010). https://doi.org/10.1007/s11103-010-9688-2

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