Specification and regulation of vascular tissue identity in the Arabidopsis embryo

ABSTRACT Development of plant vascular tissues involves tissue identity specification, growth, pattern formation and cell-type differentiation. Although later developmental steps are understood in some detail, it is still largely unknown how the tissue is initially specified. We used the early Arabidopsis embryo as a simple model to study this process. Using a large collection of marker genes, we found that vascular identity was specified in the 16-cell embryo. After a transient precursor state, however, there was no persistent uniform tissue identity. Auxin is intimately connected to vascular tissue development. We found that, although an AUXIN RESPONSE FACTOR5/MONOPTEROS (ARF5/MP)-dependent auxin response was required, it was not sufficient for tissue specification. We therefore used a large-scale enhanced yeast one-hybrid assay to identify potential regulators of vascular identity. Network and functional analysis of candidate regulators suggest that vascular identity is under robust, complex control. We found that one candidate regulator, the G-class bZIP transcription factor GBF2, can modulate vascular gene expression by tuning MP output through direct interaction. Our work uncovers components of a gene regulatory network that controls the initial specification of vascular tissue identity. Highlighted Article: Vascular tissues are the first to form in the plant embryo. Using a yeast one hybrid assay, we identify that GBF2 acts as a vascular gene expression modulator, via interactions with auxin response factors.

[1]  Xiyan Yang,et al.  A PXY-Mediated Transcriptional Network Integrates Signaling Mechanisms to Control Vascular Development in Arabidopsis[OPEN]. , 2020, The Plant cell.

[2]  I. Grosse,et al.  A single ChIP-seq dataset is sufficient for comprehensive analysis of motifs co-occurrence with MCOT package , 2019, Nucleic acids research.

[3]  D. Dickel,et al.  High-Throughput Single-Cell Transcriptome Profiling of Plant Cell Types , 2019, Cell reports.

[4]  K. Nieselt,et al.  Spatiotemporal Developmental Trajectories in the Arabidopsis Root Revealed Using High-Throughput Single-Cell RNA Sequencing. , 2019, Developmental cell.

[5]  H. Kang,et al.  Single-Cell RNA Sequencing Resolves Molecular Relationships Among Individual Plant Cells1[OPEN] , 2019, Plant Physiology.

[6]  Ari Pekka Mähönen,et al.  Mobile PEAR transcription factors integrate positional cues to prime cambial growth , 2019, Nature.

[7]  Ari Pekka Mähönen,et al.  High levels of auxin signalling define the stem-cell organizer of the vascular cambium , 2019, Nature.

[8]  Richard S. Smith,et al.  A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis , 2018, Nature Plants.

[9]  Daniel E. Runcie,et al.  Transcriptional regulation of nitrogen-associated metabolism and growth , 2018, Nature.

[10]  D. Hwang,et al.  BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth , 2018, Nature Plants.

[11]  Basten L. Snoek,et al.  The Arabidopsis bZIP transcription factor family-an update. , 2018, Current opinion in plant biology.

[12]  Y. Helariutta,et al.  Phloem differentiation: an integrative model for cell specification , 2017, Journal of Plant Research.

[13]  K. T. ten Tusscher,et al.  Auxin Information Processing; Partners and Interactions beyond the Usual Suspects , 2017, International journal of molecular sciences.

[14]  Thomas J. Hardcastle,et al.  Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration , 2017, Proceedings of the National Academy of Sciences.

[15]  D. Weijers,et al.  Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo , 2017, Nature Plants.

[16]  S. Zeeman,et al.  OCTOPUS-LIKE 2, a novel player in Arabidopsis root and vascular development, reveals a key role for OCTOPUS family genes in root metaphloem sieve tube differentiation. , 2017, The New phytologist.

[17]  S. Chattopadhyay,et al.  GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana , 2017, The Plant journal : for cell and molecular biology.

[18]  I. Grosse,et al.  Diversity of cis-regulatory elements associated with auxin response in Arabidopsis thaliana , 2017, Journal of experimental botany.

[19]  J. Lohmann,et al.  Spatial specificity of auxin responses coordinates wood formation , 2017, Nature Communications.

[20]  Lan-fen Li,et al.  Crystal Structure of Tetrameric Arabidopsis MYC2 Reveals the Mechanism of Enhanced Interaction with DNA. , 2017, Cell reports.

[21]  J. Agustí,et al.  Strigolactone- and Karrikin-Independent SMXL Proteins Are Central Regulators of Phloem Formation , 2017, Current Biology.

[22]  Michael D. Nodine,et al.  Widespread Contamination of Arabidopsis Embryo and Endosperm Transcriptome Data Sets[OPEN] , 2017, Plant Cell.

[23]  D. Weijers,et al.  Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo , 2017, Proceedings of the National Academy of Sciences.

[24]  Juan Dong,et al.  Phosphorylation of the Polarity Protein BASL Differentiates Asymmetric Cell Fate through MAPKs and SPCH , 2016, Current Biology.

[25]  Ge Gao,et al.  PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants , 2016, Nucleic Acids Res..

[26]  Mathew G. Lewsey,et al.  Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape , 2016, Cell.

[27]  D. Weijers,et al.  Molecular Characterization of Arabidopsis GAL4/UAS Enhancer Trap Lines Identifies Novel Cell-Type-Specific Promoters1[OPEN] , 2016, Plant Physiology.

[28]  Jun Xiao,et al.  Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate , 2015, eLife.

[29]  Jun Xiao,et al.  Author response: Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate , 2015 .

[30]  U. Zentgraf,et al.  Phosphorylation Affects DNA-Binding of the Senescence-Regulating bZIP Transcription Factor GBF1 , 2015, Plants.

[31]  Charles W. Melnyk,et al.  A Developmental Framework for Graft Formation and Vascular Reconnection in Arabidopsis thaliana , 2015, Current Biology.

[32]  Ling Zhu,et al.  Phosphorylation of Serine 186 of bHLH Transcription Factor SPEECHLESS Promotes Stomatal Development in Arabidopsis. , 2015, Molecular plant.

[33]  Anna Akhmanova,et al.  Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification , 2015, Plant Cell.

[34]  G. Ditta,et al.  microRNA regulation of fruit growth , 2015, Nature Plants.

[35]  T. Vernoux,et al.  Primers used in this study. , 2015 .

[36]  M. Schmid,et al.  Cell type-specific transcriptome analysis in the early Arabidopsis thaliana embryo , 2014, Development.

[37]  Jason A. Corwin,et al.  An Arabidopsis Gene Regulatory Network for Secondary Cell Wall Synthesis , 2014, Nature.

[38]  M. Sugiyama,et al.  A novel system for xylem cell differentiation in Arabidopsis thaliana. , 2014, Molecular plant.

[39]  Jessica K. Chang,et al.  Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells , 2014, Science.

[40]  H. Fukuda,et al.  A bHLH Complex Activates Vascular Cell Division via Cytokinin Action in Root Apical Meristem , 2014, Current Biology.

[41]  D. Wagner,et al.  Integration of growth and patterning during vascular tissue formation in Arabidopsis , 2014, Science.

[42]  Y. Kang,et al.  Molecular genetic framework for protophloem formation , 2014, Proceedings of the National Academy of Sciences.

[43]  W. Dröge-Laser,et al.  The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery , 2014, Nature Communications.

[44]  P. Prusinkiewicz,et al.  Genetic control of plant development by overriding a geometric division rule. , 2014, Developmental cell.

[45]  Teva Vernoux,et al.  Structural basis for oligomerization of auxin transcriptional regulators , 2014, Nature Communications.

[46]  Richard S. Smith,et al.  Modeling Framework for the Establishment of the Apical-Basal Embryonic Axis in Plants , 2013, Current Biology.

[47]  S. Turner,et al.  WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation , 2013, Development.

[48]  H. Fukuda,et al.  An atypical bHLH transcription factor regulates early xylem development downstream of auxin. , 2013, Plant & cell physiology.

[49]  Pierre Barbier de Reuille,et al.  A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. , 2013, Developmental cell.

[50]  S. Brady,et al.  Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed , 2013, Proceedings of the National Academy of Sciences.

[51]  Klaus Harter,et al.  Bioinformatic cis-element analyses performed in Arabidopsis and rice disclose bZIP- and MYB-related binding sites as potential AuxRE-coupling elements in auxin-mediated transcription , 2012, BMC Plant Biology.

[52]  U. Sauer,et al.  Redox-mediated Mechanisms Regulate DNA Binding Activity of the G-group of Basic Region Leucine Zipper (bZIP) Transcription Factors in Arabidopsis* , 2012, The Journal of Biological Chemistry.

[53]  Aparna Singh,et al.  Molecular Interactions of GBF1 with HY5 and HYH Proteins during Light-mediated Seedling Development in Arabidopsis thaliana* , 2012, The Journal of Biological Chemistry.

[54]  G. Zheng,et al.  Graft-union development: a delicate process that involves cell–cell communication between scion and stock for local auxin accumulation , 2012, Journal of experimental botany.

[55]  Wenzislava Ckurshumova,et al.  Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. , 2012, The New phytologist.

[56]  Jan Willem Borst,et al.  Different auxin response machineries control distinct cell fates in the early plant embryo. , 2012, Developmental cell.

[57]  Doreen Ware,et al.  Enhanced Y1H assays for Arabidopsis , 2011, Nature Methods.

[58]  Bryan Lajoie,et al.  Enhanced yeast one-hybrid (eY1H) assays for high-throughput gene-centered regulatory network mapping , 2011, Nature Methods.

[59]  Ykä Helariutta,et al.  A Mutually Inhibitory Interaction between Auxin and Cytokinin Specifies Vascular Pattern in Roots , 2011, Current Biology.

[60]  D. Weijers,et al.  A Versatile Set of Ligation-Independent Cloning Vectors for Functional Studies in Plants1[C][W][OA] , 2011, Plant Physiology.

[61]  C. Perrot-Rechenmann,et al.  AUXIN RESPONSE FACTOR8 Regulates Arabidopsis Petal Growth by Interacting with the bHLH Transcription Factor BIGPETALp[C][W] , 2011, Plant Cell.

[62]  E. Scarpella,et al.  Simultaneous activation of SHR and ATHB8 expression defines switch to preprocambial cell state in Arabidopsis leaf development , 2011, Developmental dynamics : an official publication of the American Association of Anatomists.

[63]  H. Fukuda,et al.  TDIF Peptide Signaling Regulates Vascular Stem Cell Proliferation via the WOX4 Homeobox Gene in Arabidopsis[W] , 2010, Plant Cell.

[64]  T. Demura,et al.  VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System1[W] , 2010, Plant Physiology.

[65]  Ykä Helariutta,et al.  Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate , 2010, Nature.

[66]  U. Zentgraf,et al.  G-Box Binding Factor1 Reduces CATALASE2 Expression and Regulates the Onset of Leaf Senescence in Arabidopsis1[W][OA] , 2010, Plant Physiology.

[67]  M. Schmid,et al.  MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor , 2010, Nature.

[68]  Lan-Ying Lee,et al.  Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method , 2009, Plant Methods.

[69]  R. Zhong,et al.  MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. , 2009, Plant & cell physiology.

[70]  Enrico Scarpella,et al.  Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves , 2009, Development.

[71]  Matthew R. Tucker,et al.  Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo , 2008, Development.

[72]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[73]  Daniel P. Schachtman,et al.  The Arabidopsis Transcription Factor MYB77 Modulates Auxin Signal Transduction[W] , 2007, The Plant Cell Online.

[74]  Eric Bonnet,et al.  A Tandem Affinity Purification-based Technology Platform to Study the Cell Cycle Interactome in Arabidopsis thaliana*S , 2007, Molecular & Cellular Proteomics.

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

[76]  Vandana Yadav,et al.  A Basic Leucine Zipper Transcription Factor, G-box-binding Factor 1, Regulates Blue Light-mediated Photomorphogenic Growth in Arabidopsis* , 2006, Journal of Biological Chemistry.

[77]  Yunde Zhao,et al.  Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. , 2006, Genes & development.

[78]  J. Friml,et al.  Control of leaf vascular patterning by polar auxin transport. , 2006, Genes & development.

[79]  Uwe Ohler,et al.  Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[80]  G. Jürgens,et al.  Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. , 2006, Developmental cell.

[81]  Masayuki Higuchi,et al.  Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development , 2006, Science.

[82]  Tetsuro Mimura,et al.  Transcription switches for protoxylem and metaxylem vessel formation. , 2005, Genes & development.

[83]  Vincent Colot,et al.  Profiling histone modification patterns in plants using genomic tiling microarrays , 2005, Nature Methods.

[84]  J. Ecker,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[85]  C. Bernhardt,et al.  The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis , 2005, Development.

[86]  Ana I. Caño-Delgado,et al.  Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1) , 2004, The Plant Cell Online.

[87]  Klaus Harter,et al.  Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. , 2004, The Plant journal : for cell and molecular biology.

[88]  E. Meyerowitz,et al.  The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development , 2004, Development.

[89]  Ari Pekka Mähönen,et al.  APL regulates vascular tissue identity in Arabidopsis , 2003, Nature.

[90]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[91]  Wenzislava Ckurshumova,et al.  Auxin Signaling in Arabidopsis Leaf Vascular Development1 , 2003, Plant Physiology.

[92]  R. Simon,et al.  The DORNRÖSCHEN/ENHANCER OF SHOOT REGENERATION1 Gene of Arabidopsis Acts in the Control of Meristem Cell Fate and Lateral Organ Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009480. , 2003, The Plant Cell Online.

[93]  Y. Komeda,et al.  Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis , 2003, Development.

[94]  G. Jürgens,et al.  The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. , 2002, Genes & development.

[95]  Chang‐Deng Hu,et al.  Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. , 2002, Molecular cell.

[96]  E. Grotewold,et al.  MYB transcription factors in Arabidopsis. , 2002, Trends in plant science.

[97]  S. Tabata,et al.  ARR1, a Transcription Factor for Genes Immediately Responsive to Cytokinins , 2001, Science.

[98]  D. Weijers,et al.  An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. , 2001, Development.

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

[100]  E. Wisman,et al.  The arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. , 2001, Plant physiology.

[101]  Ari Pekka Mähönen,et al.  A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. , 2000, Genes & development.

[102]  J. Schiefelbein,et al.  WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning , 1999, Cell.

[103]  Alan Marchant,et al.  AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues , 1999, The EMBO journal.

[104]  G. Jürgens,et al.  The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. , 1999, Development.

[105]  S. Hake,et al.  Genetic control of plant development , 1998 .

[106]  C. Hardtke,et al.  The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development , 1998, The EMBO journal.

[107]  H Fujisawa,et al.  Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. , 1997, The Plant cell.

[108]  K. Feldmann,et al.  Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism , 1996, Science.

[109]  G. Hagen,et al.  Composite structure of auxin response elements. , 1995, The Plant cell.

[110]  G. Jürgens,et al.  The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo , 1993 .

[111]  W. Terzaghi,et al.  DNA binding site preferences and transcriptional activation properties of the Arabidopsis transcription factor GBF1. , 1992, The EMBO journal.

[112]  L. Klimczak,et al.  DNA binding activity of the Arabidopsis G-box binding factor GBF1 is stimulated by phosphorylation by casein kinase II from broccoli. , 1992, The Plant cell.

[113]  T. Berleth,et al.  Mutations affecting body organization in the Arabidopsis embryo , 1991, Nature.

[114]  T. Sachs,et al.  Polarity and the Induction of Organized Vascular Tissues , 1969 .

[115]  R. Wetmore,et al.  EXPERIMENTAL INDUCTION OF VASCULAR TISSUES IN CALLUS OF ANGIOSPERMS , 1963 .

[116]  W. P. Jacobs.  THE ROLE OF AUXIN IN DIFFERENTIATION OF XYLEM AROUND A WOUND , 1952 .

[117]  S. Brady,et al.  Identification of Protein-DNA Interactions Using Enhanced Yeast One-Hybrid Assays and a Semiautomated Approach. , 2017, Methods in molecular biology.

[118]  D. Weijers,et al.  In Vivo Identification of Plant Protein Complexes Using IP-MS/MS. , 2017, Methods in molecular biology.

[119]  D. Weijers,et al.  Ligation-independent cloning for plant research. , 2015, Methods in molecular biology.

[120]  W. Edelmann,et al.  Seamless Ligation Cloning Extract (SLiCE) cloning method. , 2014, Methods in molecular biology.

[121]  D. Weijers,et al.  Imaging of phenotypes, gene expression, and protein localization during embryonic root formation in Arabidopsis. , 2013, Methods in molecular biology.

[122]  C. Scutt,et al.  Evolution of the ARF gene family in land plants: old domains, new tricks. , 2013, Molecular biology and evolution.

[123]  Gerhard K. H. Przemeck,et al.  Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization , 2004, Planta.

[124]  G. Vachon,et al.  GeBP, the first member of a new gene family in Arabidopsis, encodes a nuclear protein with DNA-binding activity and is regulated by KNAT1. , 2003, The Plant journal : for cell and molecular biology.

[125]  F. Parcy,et al.  bZIP transcription factors in Arabidopsis. , 2002, Trends in plant science.

[126]  J. Sánchez-Serrano,et al.  Wound signalling in plants. , 2001, Journal of experimental botany.

[127]  J. Haseloff,et al.  GFP variants for multispectral imaging of living cells. , 1999, Methods in cell biology.

[128]  P. Benfey,et al.  Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis , 1995 .

[129]  B. Scheres,et al.  Analysis of Root Development in Arabidopsis Thaliana , 1994 .

[130]  T. Sachs.  The Control of the Patterned Differentiation of Vascular Tissues , 1981 .