Partitioning the Apical Domain of the Arabidopsis Embryo Requires the BOBBER1 NudC Domain Protein[W][OA]

The apical domain of the embryo is partitioned into distinct regions that will give rise to the cotyledons and the shoot apical meristem. In this article, we describe a novel screen to identify Arabidopsis thaliana embryo arrest mutants that are defective in this partitioning, and we describe the phenotype of one such mutant, bobber1. bobber1 mutants arrest at the globular stage of development, they express the meristem-specific SHOOTMERISTEMLESS gene throughout the top half of the embryo, and they fail to express the AINTEGUMENTA transcript normally found in cotyledons. Thus, BOBBER1 is required to limit the extent of the meristem domain and/or to promote the development of the cotyledon domains. Based on expression of early markers for apical development, bobber1 mutants differentiate protodermis and undergo normal early apical development. Consistent with a role for auxin in cotyledon development, BOBBER1 mutants fail to express localized maxima of the DR5:green fluorescent protein reporter. BOBBER1 encodes a protein with homology to the Aspergillus nidulans protein NUDC that has similarity to protein chaperones, indicating a possible role for BOBBER1 in synthesis or transport of proteins involved in patterning the Arabidopsis embryo.

[1]  J. López,et al.  BOBBER1 Is a Noncanonical Arabidopsis Small Heat Shock Protein Required for Both Development and Thermotolerance[W][OA] , 2009, Plant Physiology.

[2]  G. Braus,et al.  The Nuclear Migration Protein NUDF/LIS1 Forms a Complex with NUDC and BNFA at Spindle Pole Bodies , 2008, Eukaryotic Cell.

[3]  J. Long,et al.  TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis , 2008, Science.

[4]  Michael D. Nodine,et al.  Two receptor-like kinases required together for the establishment of Arabidopsis cotyledon primordia. , 2008, Developmental biology.

[5]  M. Freeling,et al.  How to usefully compare homologous plant genes and chromosomes as DNA sequences. , 2008, The Plant journal : for cell and molecular biology.

[6]  W. Lukowitz,et al.  Talk global, act local-patterning the Arabidopsis embryo. , 2008, Current opinion in plant biology.

[7]  K. Caldwell,et al.  The microtubule-associated protein, NUD-1, exhibits chaperone activity in vitro , 2008, Cell Stress and Chaperones.

[8]  Yunde Zhao,et al.  NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[9]  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.

[10]  Elliot M. Meyerowitz,et al.  Antagonistic Regulation of PIN Phosphorylation by PP2A and PINOID Directs Auxin Flux , 2007, Cell.

[11]  Michael D. Nodine,et al.  RPK1 and TOAD2 are two receptor-like kinases redundantly required for arabidopsis embryonic pattern formation. , 2007, Developmental cell.

[12]  Brian C. Thomas,et al.  G-Boxes, Bigfoot Genes, and Environmental Response: Characterization of Intragenomic Conserved Noncoding Sequences in Arabidopsis[W] , 2007, The Plant Cell Online.

[13]  K. Hibara,et al.  Arabidopsis CUP-SHAPED COTYLEDON3 Regulates Postembryonic Shoot Meristem and Organ Boundary Formation[W] , 2006, The Plant Cell Online.

[14]  Xiaoqi Liu,et al.  A mammalian NudC-like protein essential for dynein stability and cell viability. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Barton,et al.  Interactions between the Cell Cycle and Embryonic Patterning in Arabidopsis Uncovered by a Mutation in DNA Polymerase ε[W][OA] , 2005, The Plant Cell Online.

[16]  E. Glawischnig,et al.  The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo , 2005, Development.

[17]  M. Barton,et al.  Surge and destroy: the role of auxin in plant embryogenesis , 2005, Development.

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

[19]  T. Vernoux,et al.  PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis , 2004, Development.

[20]  B. Hoffmann,et al.  The LIS1-related protein NUDF of Aspergillus nidulans and its interaction partner NUDE bind directly to specific subunits of dynein and dynactin and to alpha- and gamma-tubulin. , 2004, The Journal of biological chemistry.

[21]  S. Reddy,et al.  Multiple cis-Elements Mediate the Transcriptional Activation of Human fra-1 by 12-O-Tetradecanoylphorbol-13-acetate in Bronchial Epithelial Cells* , 2003, Journal of Biological Chemistry.

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

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

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

[25]  S. D. de Vries,et al.  The CUP-SHAPED COTYLEDON3 Gene Is Required for Boundary and Shoot Meristem Formation in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012203. , 2003, The Plant Cell Online.

[26]  K. Caldwell,et al.  Role for NudC, a dynein-associated nuclear movement protein, in mitosis and cytokinesis , 2003, Journal of Cell Science.

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

[28]  Dyneins Motor on in Plants , 2002, Traffic.

[29]  A. Valencia,et al.  p23 and HSP20/α‐crystallin proteins define a conserved sequence domain present in other eukaryotic protein families , 2002, FEBS letters.

[30]  E. Meyerowitz,et al.  Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. , 2002, Development.

[31]  M. Razzaque,et al.  Involvement of the fungal nuclear migration gene nudC human homolog in cell proliferation and mitotic spindle formation. , 2002, Experimental cell research.

[32]  S. Mcconnell,et al.  NudC Associates with Lis1 and the Dynein Motor at the Leading Pole of Neurons , 2001, The Journal of Neuroscience.

[33]  B. Hoffmann,et al.  The LIS1-related Protein NUDF of Aspergillus nidulans and Its Interaction Partner NUDE Bind Directly to Specific Subunits of Dynein and Dynactin and to α- and γ-Tubulin* , 2001, The Journal of Biological Chemistry.

[34]  J. Buchner,et al.  Hsp90: Chaperoning signal transduction , 2001, Journal of cellular physiology.

[35]  C. Helliwell,et al.  The Arabidopsis AMP1 Gene Encodes a Putative Glutamate Carboxypeptidase , 2001, The Plant Cell Online.

[36]  R. N. Morris,et al.  Evolutionarily conserved nuclear migration genes required for early embryonic development in Caenorhabditiselegans , 2001, Development Genes and Evolution.

[37]  Carolyn J. Lawrence-Dill,et al.  Dyneins Have Run Their Course in Plant Lineage , 2001, Traffic.

[38]  K. Hibara,et al.  The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. , 2001, Development.

[39]  Y. Nakamura,et al.  Structural analysis of Arabidopsis thaliana chromosome 5. X. Sequence features of the regions of 3,076,755 bp covered by sixty P1 and TAC clones. , 2000, DNA research : an international journal for rapid publication of reports on genes and genomes.

[40]  N. Morris,et al.  Isolation of a new set of Aspergillus nidulans mutants defective in nuclear migration , 1999, Current Genetics.

[41]  M. Aida,et al.  Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. , 1999, Development.

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

[43]  S. Beckwith,et al.  The “8-kD” Cytoplasmic Dynein Light Chain Is Required for Nuclear Migration and for Dynein Heavy Chain Localization in Aspergillus nidulans , 1998, The Journal of cell biology.

[44]  J. Thompson,et al.  Multiple sequence alignment with Clustal X. , 1998, Trends in biochemical sciences.

[45]  J. Long,et al.  The development of apical embryonic pattern in Arabidopsis. , 1998, Development.

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

[47]  G. Eichele,et al.  The lissencephaly gene product Lis1, a protein involved in neuronal migration, interacts with a nuclear movement protein, NudC , 1998, Current Biology.

[48]  T. Thomas,et al.  PEI1, an Embryo-Specific Zinc Finger Protein Gene Required for Heart-Stage Embryo Formation in Arabidopsis , 1998, Plant Cell.

[49]  G. Neuhaus,et al.  Auxin-induced developmental patterns in Brassica juncea embryos. , 1998, Development.

[50]  N. Morris,et al.  Deletion of nudC, a nuclear migration gene of Aspergillus nidulans, causes morphological and cell wall abnormalities and is lethal. , 1997, Molecular biology of the cell.

[51]  R. Warrior,et al.  Characterization of DnudC, the Drosophila homolog of an Aspergillus gene that functions in nuclear motility , 1997, Mechanisms of Development.

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

[53]  S. Morris,et al.  A prolactin-inducible T cell gene product is structurally similar to the Aspergillus nidulans nuclear movement protein NUDC. , 1997, Molecular endocrinology.

[54]  Detlef Weigel,et al.  A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS , 1997, Current Biology.

[55]  R. Porat,et al.  Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. , 1996, The Plant cell.

[56]  C. Fischer,et al.  Influence of auxin on the establishment of bilateral symmetry in monocots , 1996 .

[57]  P. Perez,et al.  AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. , 1996, The Plant cell.

[58]  June I. Medford,et al.  A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis , 1996, Nature.

[59]  S. Osmani,et al.  NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. , 1995, Molecular biology of the cell.

[60]  N. Morris,et al.  Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[61]  E. Dennis,et al.  amp1 ‐ a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering , 1993 .

[62]  R. Poethig,et al.  Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant , 1993 .

[63]  F. Ausubel,et al.  A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. , 1993, The Plant journal : for cell and molecular biology.

[64]  N. Morris,et al.  Mitotic gold in a mold: Aspergillus genetics and the biology of mitosis. , 1992, Trends in genetics : TIG.

[65]  K. Edwards,et al.  A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. , 1991, Nucleic acids research.

[66]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[67]  S. Osmani,et al.  The molecular cloning and identification of a gene product specifically required for nuclear movement in Aspergillus nidulans , 1990, The Journal of cell biology.

[68]  Eugene W. Myers,et al.  Basic local alignment search tool. Journal of Molecular Biology , 1990 .

[69]  N. Morris.  A temperature-sensitive mutant of Aspergillus nidulans reversibly blocked in nuclear division. , 1976, Experimental cell research.

[70]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .