Genome-Wide Identification of KANADI1 Target Genes

Plant organ development and polarity establishment is mediated by the action of several transcription factors. Among these, the KANADI (KAN) subclade of the GARP protein family plays important roles in polarity-associated processes during embryo, shoot and root patterning. In this study, we have identified a set of potential direct target genes of KAN1 through a combination of chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) and genome-wide transcriptional profiling using tiling arrays. Target genes are over-represented for genes involved in the regulation of organ development as well as in the response to auxin. KAN1 affects directly the expression of several genes previously shown to be important in the establishment of polarity during lateral organ and vascular tissue development. We also show that KAN1 controls through its target genes auxin effects on organ development at different levels: transport and its regulation, and signaling. In addition, KAN1 regulates genes involved in the response to abscisic acid, jasmonic acid, brassinosteroids, ethylene, cytokinins and gibberellins. The role of KAN1 in organ polarity is antagonized by HD-ZIPIII transcription factors, including REVOLUTA (REV). A comparison of their target genes reveals that the REV/KAN1 module acts in organ patterning through opposite regulation of shared targets. Evidence of mutual repression between closely related family members is also shown.

[1]  Ilha Lee,et al.  HD-ZIP III Activity Is Modulated by Competitive Inhibitors via a Feedback Loop in Arabidopsis Shoot Apical Meristem Development[W] , 2008, The Plant Cell Online.

[2]  E. Meyerowitz,et al.  Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem , 2005, Current Biology.

[3]  F. Nogueira,et al.  Pattern formation via small RNA mobility. , 2009, Genes & development.

[4]  J. Bowman,et al.  KANADI and Class III HD-Zip Gene Families Regulate Embryo Patterning and Modulate Auxin Flow during Embryogenesis in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[5]  Yunde Zhao,et al.  NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis , 2008, Proceedings of the National Academy of Sciences.

[6]  Rongcheng Lin,et al.  Two Homologous ATP-Binding Cassette Transporter Proteins, AtMDR1 and AtPGP1, Regulate Arabidopsis Photomorphogenesis and Root Development by Mediating Polar Auxin Transport1 , 2005, Plant Physiology.

[7]  Y. Eshed,et al.  Auxin Response Factors Mediate Arabidopsis Organ Asymmetry via Modulation of KANADI Activityw⃞ , 2005, The Plant Cell Online.

[8]  J. Bowman,et al.  Differentiating Arabidopsis Shoots from Leaves by Combined YABBY Activities[W][OA] , 2010, Plant Cell.

[9]  J. R. McConnell,et al.  Leaf polarity and meristem formation in Arabidopsis. , 1998, Development.

[10]  P. Springer,et al.  KANADI1 regulates adaxial–abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2 , 2008, Proceedings of the National Academy of Sciences.

[11]  R. Brandt,et al.  ATHB4 and HAT3, two class II HD-ZIP transcription factors, control leaf development in Arabidopsis , 2012, Plant signaling & behavior.

[12]  Maitreya J. Dunham,et al.  Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis , 2000, Nature.

[13]  B. Reinhart,et al.  Of blades and branches: understanding and expanding the Arabidopsis ad/abaxial regulatory network through target gene identification. , 2012, Cold Spring Harbor symposia on quantitative biology.

[14]  J. Bowman,et al.  Establishment of polarity in lateral organs of plants , 2001, Current Biology.

[15]  D. Shibata,et al.  FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. , 1999, Genes & development.

[16]  J. Bowman,et al.  Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots , 2001, Nature.

[17]  H. Tsukaya,et al.  The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. , 2002, Plant & cell physiology.

[18]  Xuemei Chen,et al.  Orchestration of the Floral Transition and Floral Development in Arabidopsis by the Bifunctional Transcription Factor APETALA2[W][OA] , 2010, Plant Cell.

[19]  Adam M. Gustafson,et al.  microRNA-Directed Phasing during Trans-Acting siRNA Biogenesis in Plants , 2005, Cell.

[20]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[21]  S. Tiwari,et al.  Aux/IAA Proteins Contain a Potent Transcriptional Repression Domain , 2004, The Plant Cell Online.

[22]  G. Haughn,et al.  The Arabidopsis BEL1-LIKE HOMEODOMAIN Proteins SAW1 and SAW2 Act Redundantly to Regulate KNOX Expression Spatially in Leaf Margins[W] , 2007, The Plant Cell Online.

[23]  J. Bowman,et al.  Patterning and polarity in seed plant shoots. , 2008, Annual review of plant biology.

[24]  J. Bowman,et al.  Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation , 2010, Development.

[25]  Youn-sung Kim,et al.  microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. , 2005, The Plant journal : for cell and molecular biology.

[26]  Y. Machida,et al.  Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. , 2007, The Plant journal : for cell and molecular biology.

[27]  S. Turner,et al.  PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development , 2007, Current Biology.

[28]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[29]  J. Long,et al.  Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors , 2010, Nature.

[30]  Yunde Zhao,et al.  NPY genes play an essential role in root gravitropic responses in Arabidopsis. , 2011, Molecular plant.

[31]  B. Reinhart,et al.  MicroRNAs in plants. , 2002, Genes & development.

[32]  M. Barton,et al.  A Feedback Regulatory Module Formed by LITTLE ZIPPER and HD-ZIPIII Genes[W][OA] , 2007, The Plant Cell Online.

[33]  D. Leister,et al.  Plastocyanin Is Indispensable for Photosynthetic Electron Flow in Arabidopsis thaliana* , 2003, Journal of Biological Chemistry.

[34]  R. Kerstetter,et al.  KANADI regulates organ polarity in Arabidopsis , 2001, Nature.

[35]  L. Lehle,et al.  The Auxin-induced Maize Gene ZmSAUR2 Encodes a Short-lived Nuclear Protein Expressed in Elongating Tissues* , 2003, Journal of Biological Chemistry.

[36]  Tom Beeckman,et al.  Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression , 2005, Development.

[37]  Hiroo Fukuda,et al.  Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system , 2008, Proceedings of the National Academy of Sciences.

[38]  Y. Eshed,et al.  Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis , 2013, Development.

[39]  J. Reed,et al.  Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. , 2012, The Plant journal : for cell and molecular biology.

[40]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[41]  J L Bowman,et al.  Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. , 1999, Development.

[42]  Jeongmoo Park,et al.  LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis , 2006, Development.

[43]  S. Lucchetti,et al.  The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. , 1995, Development.

[44]  B. Poovaiah,et al.  Molecular and Biochemical Evidence for the Involvement of Calcium/Calmodulin in Auxin Action* , 2000, The Journal of Biological Chemistry.

[45]  G. Jürgens,et al.  Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. , 1999, Science.

[46]  M. Prigge,et al.  REVOLUTA regulates meristem initiation at lateral positions. , 2001, The Plant journal : for cell and molecular biology.

[47]  Guiliang Tang,et al.  MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region , 2004 .

[48]  B. Causier,et al.  The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[49]  J. Bowman,et al.  Distinct Mechanisms Promote Polarity Establishment in Carpels of Arabidopsis , 1999, Cell.

[50]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[51]  G. Falasca,et al.  Auxin Regulates Arabidopsis Anther Dehiscence, Pollen Maturation, and Filament Elongation[W] , 2008, The Plant Cell Online.

[52]  Klaus Palme,et al.  AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis , 2002, Cell.

[53]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

[54]  S. H. Lee,et al.  Phospholipase A2 Is Required for PIN-FORMED Protein Trafficking to the Plasma Membrane in the Arabidopsis Root[C][W] , 2010, Plant Cell.

[55]  J. Bowman,et al.  Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities , 2004, Development.

[56]  D. Weijers,et al.  The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. , 2001, Development.

[57]  T. Koshiba,et al.  The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[58]  G. Hagen,et al.  The Roles of Auxin Response Factor Domains in Auxin-Responsive Transcription Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008417. , 2003, The Plant Cell Online.

[59]  B. Reinhart,et al.  Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. , 2012, The Plant journal : for cell and molecular biology.

[60]  M. Estelle,et al.  Complex regulation of the TIR1/AFB family of auxin receptors , 2009, Proceedings of the National Academy of Sciences.

[61]  Ann E. Loraine,et al.  The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets , 2009, Bioinform..

[62]  Masahiko Furutani,et al.  The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level , 2007, Development.

[63]  E. Spalding.  Diverting the downhill flow of auxin to steer growth during tropisms. , 2013, American journal of botany.

[64]  D. Inzé,et al.  The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. , 2012, The Plant journal : for cell and molecular biology.

[65]  T. Vernoux,et al.  PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. , 2000, Development.

[66]  Michelle T. Juarez,et al.  microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity , 2004, Nature.

[67]  J. Bowman,et al.  Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes , 2003, Current Biology.

[68]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[69]  M. Bennett,et al.  The Binding of Auxin to the Arabidopsis Auxin Influx Transporter AUX11[OA] , 2008, Plant Physiology.

[70]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[71]  Karen S. Osmont,et al.  A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Klaus Palme,et al.  A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux , 2004, Science.

[73]  J. Bowman,et al.  Roles for Class III HD-Zip and KANADI Genes in Arabidopsis Root Development1 , 2004, Plant Physiology.