SWI3 Subunits of Putative SWI/SNF Chromatin-Remodeling Complexes Play Distinct Roles during Arabidopsis Developmentw⃞

SWITCH/SUCROSE NONFERMENTING (SWI/SNF) chromatin-remodeling complexes mediate ATP-dependent alterations of DNA–histone contacts. The minimal functional core of conserved SWI/SNF complexes consists of a SWI2/SNF2 ATPase, SNF5, SWP73, and a pair of SWI3 subunits. Because of early duplication of the SWI3 gene family in plants, Arabidopsis thaliana encodes four SWI3-like proteins that show remarkable functional diversification. Whereas ATSWI3A and ATSWI3B form homodimers and heterodimers and interact with BSH/SNF5, ATSWI3C, and the flowering regulator FCA, ATSWI3D can only bind ATSWI3B in yeast two-hybrid assays. Mutations of ATSWI3A and ATSWI3B arrest embryo development at the globular stage. By a possible imprinting effect, the atswi3b mutations result in death for approximately half of both macrospores and microspores. Mutations in ATSWI3C cause semidwarf stature, inhibition of root elongation, leaf curling, aberrant stamen development, and reduced fertility. Plants carrying atswi3d mutations display severe dwarfism, alterations in the number and development of flower organs, and complete male and female sterility. These data indicate that, by possible contribution to the combinatorial assembly of different SWI/SNF complexes, the ATSWI3 proteins perform nonredundant regulatory functions that affect embryogenesis and both the vegetative and reproductive phases of plant development.

[1]  C. Peterson,et al.  Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. , 2002, Molecular cell.

[2]  R. Amasino,et al.  Regulation of Flowering Time by Histone Acetylation in Arabidopsis , 2003, Science.

[3]  R. Kingston,et al.  Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. , 1999, Molecular cell.

[4]  M. Yaniv,et al.  SWI/SNF chromatin remodeling and cancer. , 2002, Current opinion in genetics & development.

[5]  A. Lamond,et al.  hLodestar/HuF2 interacts with CDC5L and is involved in pre-mRNA splicing. , 2003, Biochemical and biophysical research communications.

[6]  C. Dean,et al.  Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting , 2004, The Plant Cell Online.

[7]  P. Zielenkiewicz,et al.  Plant chromatin — Learning fromsimilarities and differences , 2003 .

[8]  W. Gruissem,et al.  Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte , 2004, Nature.

[9]  R. Amasino,et al.  Role of chromatin modification in flowering-time control. , 2005, Trends in plant science.

[10]  Yong Li,et al.  An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics , 2003, Plant Molecular Biology.

[11]  Stuart H. Orkin,et al.  The SWI/SNF complex — chromatin and cancer , 2004, Nature Reviews Cancer.

[12]  Rossana Henriques,et al.  Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. , 2002, The Plant journal : for cell and molecular biology.

[13]  M. Yaniv,et al.  The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression , 2000, EMBO reports.

[14]  Keqiang Wu,et al.  CHB2, a member of the SWI3 gene family, is a global regulator in Arabidopsis , 2003, Plant Molecular Biology.

[15]  R. Martienssen,et al.  Dependence of Heterochromatic Histone H3 Methylation Patterns on the Arabidopsis Gene DDM1 , 2002, Science.

[16]  Paul Tempst,et al.  RSC, an Essential, Abundant Chromatin-Remodeling Complex , 1996, Cell.

[17]  R. Macknight,et al.  RNA processing and Arabidopsis flowering time control. , 2004, Biochemical Society transactions.

[18]  A. Sands,et al.  Disruption of Ini1 Leads to Peri-Implantation Lethality and Tumorigenesis in Mice , 2001, Molecular and Cellular Biology.

[19]  P. Becker.  Nucleosome sliding: facts and fiction , 2002, The EMBO journal.

[20]  L. Hennig,et al.  Chromatin-Remodeling and Memory Factors. New Regulators of Plant Development , 2002, Plant Physiology.

[21]  B. Laurent,et al.  Essential Roles of Snf5p in Snf-Swi Chromatin Remodeling In Vivo , 2001, Molecular and Cellular Biology.

[22]  ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis , 2003 .

[23]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[24]  David P. Kreil,et al.  Involvement of Putative SNF2 Chromatin Remodeling Protein DRD1 in RNA-Directed DNA Methylation , 2004, Current Biology.

[25]  A. Heck,et al.  Differential Targeting of Two Distinct SWI/SNF-Related Drosophila Chromatin-Remodeling Complexes , 2004, Molecular and Cellular Biology.

[26]  Madeline A. Crosby,et al.  The trithorax Group Genemoira Encodes a Brahma-Associated Putative Chromatin-Remodeling Factor in Drosophila melanogaster , 1999, Molecular and Cellular Biology.

[27]  D. Wagner.  Chromatin regulation of plant development. , 2003, Current opinion in plant biology.

[28]  R. Amasino,et al.  PIE1, an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012161. , 2003, The Plant Cell Online.

[29]  Szymon Kaczanowski,et al.  AtSWI3B, an Arabidopsis homolog of SWI3, a core subunit of yeast Swi/Snf chromatin remodeling complex, interacts with FCA, a regulator of flowering time. , 2002, Nucleic acids research.

[30]  N. Ohad,et al.  FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. , 2004, The Plant journal : for cell and molecular biology.

[31]  E. Meyerowitz,et al.  A Polycomb-group gene regulates homeotic gene expression in Arabidopsis , 1997, Nature.

[32]  Min Han,et al.  lin-35/Rb Cooperates With the SWI/SNF Complex to Control Caenorhabditis elegans Larval Development , 2004, Genetics.

[33]  D. Wagner,et al.  SPLAYED, a Novel SWI/SNF ATPase Homolog, Controls Reproductive Development in Arabidopsis , 2002, Current Biology.

[34]  H. Dyson,et al.  Solution structure and acetyl-lysine binding activity of the GCN5 bromodomain. , 2000, Journal of molecular biology.

[35]  Keesook Lee,et al.  Srg3, a Mouse Homolog of Yeast SWI3, Is Essential for Early Embryogenesis and Involved in Brain Development , 2001, Molecular and Cellular Biology.

[36]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[37]  Kevin Struhl,et al.  Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. , 2002, Genes & development.

[38]  Robert D. Finn,et al.  Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins , 1999, Nucleic Acids Res..

[39]  H. Tsukaya,et al.  The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana , 1998, Planta.

[40]  C. Koncz,et al.  Specialized vectors for gene tagging and expression studies , 1994 .

[41]  J. A. Jarillo,et al.  Regulation of flowering time by FVE, a retinoblastoma-associated protein , 2004, Nature Genetics.

[42]  A. Spurr.  A low-viscosity epoxy resin embedding medium for electron microscopy. , 1969, Journal of ultrastructure research.

[43]  F Randazzo,et al.  A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. , 2000, Molecular cell.

[44]  J. Bowman,et al.  The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering , 2004, Development.

[45]  F. Winston,et al.  Recent advances in understanding chromatin remodeling by Swi/Snf complexes. , 2003, Current opinion in genetics & development.

[46]  R. Farràs,et al.  SKP1–SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase , 2001, The EMBO journal.

[47]  J. Paszkowski,et al.  Disruption of the plant gene MOM releases transcriptional silencing of methylated genes , 2000, Nature.

[48]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[49]  J. Jeddeloh,et al.  Maintenance of genomic methylation requires a SWI2/SNF2-like protein , 1999, Nature Genetics.

[50]  R. Macknight,et al.  Functional Significance of the Alternative Transcript Processing of the Arabidopsis Floral Promoter FCA Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010456. , 2002, The Plant Cell Online.

[51]  C. Somerville,et al.  PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[52]  G. Benvenuto,et al.  The INO80 protein controls homologous recombination in Arabidopsis thaliana. , 2004, Molecular cell.

[53]  Gerco C Angenent,et al.  Conservation and diversity in flower land. , 2004, Current opinion in plant biology.

[54]  P. Sudarsanam,et al.  The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. , 2000, Trends in genetics : TIG.

[55]  A. Jerzmanowski,et al.  Deficient in DNA Methylation 1 (DDM1) Defines a Novel Family of Chromatin-remodeling Factors* , 2003, The Journal of Biological Chemistry.

[56]  M S Waterman,et al.  Identification of common molecular subsequences. , 1981, Journal of molecular biology.

[57]  E. Richards,et al.  Chromatin remodeling in plants. , 2001, Current opinion in plant biology.

[58]  I. Henderson,et al.  Control of Arabidopsis flowering: the chill before the bloom , 2004, Development.

[59]  A. Jerzmanowski,et al.  Identification and analysis of the Arabidopsis thaliana BSH gene, a member of the SNF5 gene family. , 1999, Nucleic acids research.

[60]  W. Peacock,et al.  Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. , 2000, Proceedings of the National Academy of Sciences of the United States of America.