CLAVATA-WUSCHEL signaling in the shoot meristem

Shoot meristems are maintained by pluripotent stem cells that are controlled by CLAVATA-WUSCHEL feedback signaling. This pathway, which coordinates stem cell proliferation with differentiation, was first identified in Arabidopsis, but appears to be conserved in diverse higher plant species. In this Review, we highlight the commonalities and differences between CLAVATA-WUSCHEL pathways in different species, with an emphasis on Arabidopsis, maize, rice and tomato. We focus on stem cell control in shoot meristems, but also briefly discuss the role of these signaling components in root meristems. Summary: This Review discusses how CLV-WUS signaling coordinates stem cell proliferation with differentiation, highlighting commonalities and differences between CLV-WUS pathways in different species.

[1]  W. Werr,et al.  The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. , 2006, Molecular biology and evolution.

[2]  C. Henzler,et al.  Molecular Mechanism for Plant Steroid Receptor Activation by Somatic Embryogenesis Co-Receptor Kinases , 2013, Science.

[3]  Stone,et al.  Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions , 1998, Plant physiology.

[4]  S. Tanksley The Genetic, Developmental, and Molecular Bases of Fruit Size and Shape Variation in Tomato , 2004, The Plant Cell Online.

[5]  Hiroo Fukuda,et al.  A Plant Peptide Encoded by CLV3 Identified by in Situ MALDI-TOF MS Analysis , 2006, Science.

[6]  Z. Lippman,et al.  A cascade of arabinosyltransferases controls shoot meristem size in tomato , 2015, Nature Genetics.

[7]  M. Kojima,et al.  WUSCHEL-RELATED HOMEOBOX4 Is Involved in Meristem Maintenance and Is Negatively Regulated by the CLE Gene FCP1 in Rice[W] , 2013, Plant Cell.

[8]  Hong Ma,et al.  The FLORAL ORGAN NUMBER4 Gene Encoding a Putative Ortholog of Arabidopsis CLAVATA3 Regulates Apical Meristem Size in Rice1[W] , 2006, Plant Physiology.

[9]  S. Clark,et al.  CLAVATA2, a regulator of meristem and organ development in Arabidopsis. , 1998, Development.

[10]  R. Simon,et al.  A Signaling Module Controlling the Stem Cell Niche in Arabidopsis Root Meristems , 2009, Current Biology.

[11]  N. Raikhel,et al.  CLV3 Is Localized to the Extracellular Space, Where It Activates the Arabidopsis CLAVATA Stem Cell Signaling Pathway Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002196. , 2002, The Plant Cell Online.

[12]  C. Nägeli,et al.  Beiträge zur wissenschaftlichen Botanik / von Carl Nägeli. , 1858 .

[13]  Y. Matsubayashi,et al.  Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. , 2015, The Plant journal : for cell and molecular biology.

[14]  P. Bonham‐Smith,et al.  Cytokinin-induced changes in CLAVATA1 and WUSCHEL expression temporally coincide with altered floral development in Arabidopsis , 2006 .

[15]  C. Seidel,et al.  Moderation of Arabidopsis Root Stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes , 2013, Current Biology.

[16]  N. Mitsukawa,et al.  The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. , 1996, The Plant cell.

[17]  M. Gifford,et al.  The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development , 2003, Development.

[18]  K. Palme,et al.  ERECTA Family Genes Regulate Auxin Transport in the Shoot Apical Meristem and Forming Leaf Primordia1[C][W][OPEN] , 2013, Plant Physiology.

[19]  Masahiro Miyoshi,et al.  Mutations associated with floral organ number in rice , 1996, Planta.

[20]  S. Hake,et al.  The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. , 2001, Genes & development.

[21]  E. van der Knaap,et al.  What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape , 2014, Front. Plant Sci..

[22]  S. Clark,et al.  POLTERGEIST and PLL1 are required for stem cell function with potential roles in cell asymmetry and auxin signaling , 2008, Communicative & integrative biology.

[23]  R. Simon,et al.  Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. , 1999, Science.

[24]  Elliot M. Meyerowitz,et al.  Cytokinin signaling as a positional cue for patterning the apical–basal axis of the growing Arabidopsis shoot meristem , 2012, Proceedings of the National Academy of Sciences.

[25]  L. Jordá,et al.  ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. , 2005, The Plant journal : for cell and molecular biology.

[26]  M. Lenhard,et al.  Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers , 2007, Nature.

[27]  V. Chickarmane,et al.  Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem , 2009, Proceedings of the National Academy of Sciences.

[28]  N. Ranc,et al.  Increase in Tomato Locule Number Is Controlled by Two Single-Nucleotide Polymorphisms Located Near WUSCHEL1[C][W] , 2011, Plant Physiology.

[29]  Paul T. Tarr,et al.  An Evolutionarily Conserved Pseudokinase Mediates Stem Cell Production in Plants , 2011, Plant Cell.

[30]  M. Yamada,et al.  BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. , 2015, The New phytologist.

[31]  J. Feijó,et al.  Hydroxyproline O‐arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens , 2015, The Plant journal : for cell and molecular biology.

[32]  J. Kyozuka,et al.  Direct control of shoot meristem activity by a cytokinin-activating enzyme , 2007, Nature.

[33]  S. Clark,et al.  The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase , 1999, Plant Cell.

[34]  J. Sheng,et al.  Identification of target ligands of CORYNE in Arabidopsis by phage display library. , 2011, Journal of integrative plant biology.

[35]  T. Laux,et al.  Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana , 2004, Development.

[36]  E. Klekowski,et al.  IMPERMANENT INITIALS OF THE SHOOT APEX AND DIPLONTIC SELECTION IN A JUNIPER CHIMERA , 1985 .

[37]  E. Meyerowitz,et al.  CLAVATA 3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA 1 , 1995 .

[38]  T. Girke,et al.  Plant stem cell maintenance involves direct transcriptional repression of differentiation program , 2013, Molecular systems biology.

[39]  S. Hake,et al.  thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase , 2005, Development.

[40]  S. Kawano,et al.  Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1[OPEN] , 2015, Plant Cell.

[41]  R. Simon,et al.  Shared and distinct functions of the pseudokinase CORYNE (CRN) in shoot and root stem cell maintenance of Arabidopsis , 2016, Journal of experimental botany.

[42]  F. Tax,et al.  CLAVATA Signaling Pathway Receptors of Arabidopsis Regulate Cell Proliferation in Fruit Organ Formation as well as in Meristems , 2011, Genetics.

[43]  E. Meyerowitz,et al.  CLAVATA1, a regulator of meristem and flower development in Arabidopsis. , 1993, Development.

[44]  Y. Matsubayashi,et al.  Chemical Synthesis of Arabidopsis CLV3 Glycopeptide Reveals the Impact of Hydroxyproline Arabinosylation on Peptide Conformation and Activity , 2012, Plant & cell physiology.

[45]  J. Cock,et al.  A large family of genes that share homology with CLAVATA3. , 2001, Plant physiology.

[46]  Rüdiger Simon,et al.  The Receptor Kinase CORYNE of Arabidopsis Transmits the Stem Cell–Limiting Signal CLAVATA3 Independently of CLAVATA1[W] , 2008, The Plant Cell Online.

[47]  D. Jackson,et al.  Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus , 2013, Nature Genetics.

[48]  Henrik Jönsson,et al.  WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. , 2011, Genes & development.

[49]  Renze Heidstra,et al.  The 14–Amino Acid CLV3, CLE19, and CLE40 Peptides Trigger Consumption of the Root Meristem in Arabidopsis through a CLAVATA2-Dependent Pathwayw⃞ , 2005, The Plant Cell Online.

[50]  Brody J Deyoung,et al.  The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[51]  B. Je,et al.  The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size , 2013, Nature.

[52]  Qingyong Yang,et al.  A novel single-nucleotide mutation in a CLAVATA3 gene homolog controls a multilocular silique trait in Brassica rapa L. , 2014, Molecular plant.

[53]  B. Scheres,et al.  Root-Specific CLE19 Overexpression and the sol1/2 Suppressors Implicate a CLV-like Pathway in the Control of Arabidopsis Root Meristem Maintenance , 2003, Current Biology.

[54]  Horim Lee,et al.  Complexity in Differential Peptide–Receptor Signaling: Response to Segonzac et al. and Mueller et al. Commentaries[W] , 2012, Plant Cell.

[55]  Heiko Schoof,et al.  The Stem Cell Population of Arabidopsis Shoot Meristems Is Maintained by a Regulatory Loop between the CLAVATA and WUSCHEL Genes , 2000, Cell.

[56]  The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1 , 2004, Development.

[57]  Maarten Koornneef,et al.  Linkage map of Arabidopsis thaliana , 1983 .

[58]  M. Aguadé,et al.  Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. , 2000, Genetics.

[59]  Nobutaka Mitsuda,et al.  Arabidopsis WUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning[W] , 2009, The Plant Cell Online.

[60]  Linqu Han,et al.  CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. , 2010, The Plant journal : for cell and molecular biology.

[61]  S. Clark,et al.  POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. , 2000, Development.

[62]  E. C. Abbe,et al.  THE GROWTH OF THE SHOOT APEX IN MAIZE: INTERNAL FEATURES , 1951 .

[63]  Heiko Schoof,et al.  Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem , 1998, Cell.

[64]  Hitoshi Sakakibara,et al.  Studies of aberrant phyllotaxy1 Mutants of Maize Indicate Complex Interactions between Auxin and Cytokinin Signaling in the Shoot Apical Meristem1[W][OA] , 2009, Plant Physiology.

[65]  Rosangela Sozzani,et al.  Arabidopsis Homologs of the Petunia HAIRY MERISTEM Gene Are Required for Maintenance of Shoot and Root Indeterminacy1[C][W][OA] , 2010, Plant Physiology.

[66]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.

[67]  D. Jackson,et al.  Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1 , 2004, Nature.

[68]  B. Je,et al.  Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits , 2016, Nature Genetics.

[69]  H. Leyser,et al.  Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana , 1992 .

[70]  Yasukazu Nakamura,et al.  Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. , 2007, Plant & cell physiology.

[71]  Brody J Deyoung,et al.  BAM Receptors Regulate Stem Cell Specification and Organ Development Through Complex Interactions With CLAVATA Signaling , 2008, Genetics.

[72]  Paul T. Tarr,et al.  Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases , 2015, Development.

[73]  S. Clark,et al.  POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis. , 2005, Developmental biology.

[74]  Suren Felekyan,et al.  Real-time dynamics of peptide ligand–dependent receptor complex formation in planta , 2015, Science Signaling.

[75]  A. Blakeslee,et al.  Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras , 1940 .

[76]  Rüdiger Simon,et al.  Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis , 2003, Development Genes and Evolution.

[77]  T. Mandel,et al.  Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways , 2016, Development.

[78]  D. Steffensen A RECONSTRUCTION OF CELL DEVELOPMENT IN THE SHOOT APEX OF MAIZE , 1968 .

[79]  H. Kitano,et al.  Conservation and diversification of meristem maintenance mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 gene. , 2006, Plant & cell physiology.

[80]  Dorota Kwiatkowska,et al.  Dynamic and Compensatory Responses of Arabidopsis Shoot and Floral Meristems to CLV3 Signaling[W] , 2006, The Plant Cell Online.

[81]  T. Mandel,et al.  The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity , 2014, Development.

[82]  C. Kuhlemeier,et al.  Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. , 2002, Genes & development.

[83]  K. Shimamoto,et al.  Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis , 2014, EMBO reports.

[84]  Steven M. Clark,et al.  CLAVATA3 IS A SPECIFIC REGULATOR OF SHOOT AND FLORAL MERISTEM DEVELOPMENT AFFECTING THE SAME PROCESSES AS CLAVATA1 , 1995 .

[85]  M. Freeling Patterns in plant development (2nd edn) , 1990 .

[86]  K. Shinozaki,et al.  Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. , 2007, The Plant journal : for cell and molecular biology.

[87]  K. Shinozaki,et al.  Mitogen-Activated Protein Kinase Regulated by the CLAVATA Receptors Contributes to Shoot Apical Meristem Homeostasis , 2010, Plant & cell physiology.

[88]  J. Lohmann,et al.  A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis , 2014, Proceedings of the National Academy of Sciences.

[89]  Qian Qian,et al.  Natural variation at the DEP1 locus enhances grain yield in rice , 2009, Nature Genetics.

[90]  Paul T. Tarr,et al.  Control of plant stem cell function by conserved interacting transcriptional regulators , 2014, Nature.

[91]  M. Hobe,et al.  Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. , 2000, Science.

[92]  H. Fukuda,et al.  Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation , 2006, Science.

[93]  S. Tanksley,et al.  Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. , 2001, Genetics.

[94]  T. Boller,et al.  Contamination Risks in Work with Synthetic Peptides: flg22 as an Example of a Pirate in Commercial Peptide Preparations[W] , 2012, Plant Cell.

[95]  StensballeA JensenON PeckSC NhseTS Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. , 2004 .

[96]  Dominique C Bergmann,et al.  Stomatal Development and Pattern Controlled by a MAPKK Kinase , 2004, Science.

[97]  C. Seidel,et al.  Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane1[W][OA] , 2009, Plant Physiology.

[98]  Robert W. Williams,et al.  The CLAVATA1 Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis , 1997, Cell.

[99]  Y. Nagato,et al.  Ovule is a lateral organ finally differentiated from the terminating floral meristem in rice. , 2011, Developmental biology.

[100]  Paul T. Tarr,et al.  Plant Stem Cell Signaling Involves Ligand-Dependent Trafficking of the CLAVATA1 Receptor Kinase , 2011, Current Biology.

[101]  Jiehua Wang,et al.  Genome-wide characterization, expression and functional analysis of CLV3/ESR gene family in tomato , 2014, BMC Genomics.

[102]  A. Kato,et al.  The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. , 1998, The Plant journal : for cell and molecular biology.

[103]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .

[104]  Paul T. Tarr,et al.  An epidermis-driven mechanism positions and scales stem cell niches in plants , 2016, Science Advances.

[105]  Paul T. Tarr,et al.  The Shoot Apical Meristem Regulatory Peptide CLV3 Does Not Activate Innate Immunity , 2012, Plant Cell.

[106]  S. Tanksley,et al.  Evaluating the genetic basis of multiple-locule fruit in a broad cross section of tomato cultivars , 2004, Theoretical and Applied Genetics.

[107]  Myeong Min Lee,et al.  POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells , 2006, Development.

[108]  S. Clark,et al.  The Arabidopsis Stem Cell Factor POLTERGEIST Is Membrane Localized and Phospholipid Stimulated[W][OA] , 2010, Plant Cell.

[109]  J. Rembur,et al.  Duration of cell cycles in the shoot apex of Chrysanthemum segetum L. , 1977 .

[110]  Wolfgang Busch,et al.  WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators , 2005, Nature.

[111]  Y. Matsubayashi,et al.  A glycopeptide regulating stem cell fate in Arabidopsis thaliana. , 2009, Nature chemical biology.

[112]  Yuriko Osakabe,et al.  RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis , 2010, Development.

[113]  Zhenbiao Yang,et al.  The CLAVATA1 Receptor-like Kinase Requires CLAVATA3 for Its Assembly into a Signaling Complex That Includes KAPP and a Rho-Related Protein , 1999, Plant Cell.

[114]  C. Dumas,et al.  ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. , 1997, The Plant journal : for cell and molecular biology.

[115]  A. Yoshida,et al.  Functional Diversification of CLAVATA3-Related CLE Proteins in Meristem Maintenance in Rice[W][OA] , 2008, The Plant Cell Online.

[116]  Bruce D. Smith,et al.  The Molecular Genetics of Crop Domestication , 2006, Cell.

[117]  Horim Lee,et al.  Stem-cell-triggered immunity through CLV 3 p – FLS 2 signalling , 2011 .

[118]  A. Yoshida,et al.  FON2 SPARE1 Redundantly Regulates Floral Meristem Maintenance with FLORAL ORGAN NUMBER2 in Rice , 2009, PLoS genetics.