SUPPRESSOR OF FRIGIDA (SUF4) Supports Gamete Fusion via Regulating Arabidopsis EC1 Gene Expression1

In Arabidopsis, gamete fusion requires the C2H2 transcription factor SUF4, which regulates the expression of the EGG CELL1 gene family. The EGG CELL1 (EC1) gene family of Arabidopsis (Arabidopsis thaliana) comprises five members that are specifically expressed in the egg cell and redundantly control gamete fusion during double fertilization. We investigated the activity of all five EC1 promoters in promoter-deletion studies and identified SUF4 (SUPPRESSOR OF FRIGIDA4), a C2H2 transcription factor, as a direct regulator of the EC1 gene expression. In particular, we demonstrated that SUF4 binds to all five Arabidopsis EC1 promoters, thus regulating their expression. The down-regulation of SUF4 in homozygous suf4-1 ovules results in reduced EC1 expression and delayed sperm fusion, which can be rescued by expressing SUF4-β-glucuronidase under the control of the SUF4 promoter. To identify more gene products able to regulate EC1 expression together with SUF4, we performed coexpression studies that led to the identification of MOM1 (MORPHEUS’ MOLECULE1), a component of a silencing mechanism that is independent of DNA methylation marks. In mom1-3 ovules, both SUF4 and EC1 genes are down-regulated, and EC1 genes show higher levels of histone 3 lysine-9 acetylation, suggesting that MOM1 contributes to the regulation of SUF4 and EC1 gene expression.

[1]  Alan M. Moses,et al.  New BAR tools for mining expression data and exploring Cis-elements in Arabidopsis thaliana. , 2016, The Plant journal : for cell and molecular biology.

[2]  R. Guerra,et al.  Live and let die: a REM complex promotes fertilization through synergid cell death in Arabidopsis , 2016, Development.

[3]  K. Yamato,et al.  An Evolutionarily Conserved Plant RKD Factor Controls Germ Cell Differentiation , 2016, Current Biology.

[4]  J. Bowman,et al.  Marchantia MpRKD Regulates the Gametophyte-Sporophyte Transition by Keeping Egg Cells Quiescent in the Absence of Fertilization , 2016, Current Biology.

[5]  V. Sundaresan,et al.  The CKI1 Histidine Kinase Specifies the Female Gametic Precursor of the Endosperm. , 2016, Developmental cell.

[6]  Hong Ma,et al.  Analysis of Arabidopsis floral transcriptome: detection of new florally expressed genes and expansion of Brassicaceae-specific gene families , 2015, Front. Plant Sci..

[7]  G. Jürgens,et al.  Twin Plants from Supernumerary Egg Cells in Arabidopsis , 2015, Current Biology.

[8]  A. Aharoni,et al.  SEEDSTICK is a Master Regulator of Development and Metabolism in the Arabidopsis Seed Coat , 2014, PLoS genetics.

[9]  Ning Zhang,et al.  Endopolyploidization and flowering time are antagonistically regulated by checkpoint component MAD1 and immunity modulator MOS1 , 2014, Nature Communications.

[10]  W. Frommer,et al.  Male–female communication triggers calcium signatures during fertilization in Arabidopsis , 2014, Nature Communications.

[11]  Mayumi Iwasaki,et al.  Identification of genes preventing transgenerational transmission of stress-induced epigenetic states , 2014, Proceedings of the National Academy of Sciences.

[12]  Sang Yeol Lee,et al.  MED18 interaction with distinct transcription factors regulates multiple plant functions , 2014, Nature Communications.

[13]  S. Sprunck,et al.  Downregulation of egg cell-secreted EC1 is accompanied with delayed gamete fusion and polytubey , 2013, Plant signaling & behavior.

[14]  S. Masiero,et al.  Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes , 2013, BMC Plant Biology.

[15]  U. Grossniklaus,et al.  Egg Cell–Secreted EC1 Triggers Sperm Cell Activation During Double Fertilization , 2012, Science.

[16]  Andreas Lausser,et al.  Egg cell signaling by the secreted peptide ZmEAL1 controls antipodal cell fate. , 2012, Developmental cell.

[17]  D. Farber,et al.  Sequence-Specific Binding of Recombinant Zbed4 to DNA: Insights into Zbed4 Participation in Gene Transcription and Its Association with Other Proteins , 2012, PloS one.

[18]  S. Sprunck,et al.  LACHESIS-dependent egg-cell signaling regulates the development of female gametophytic cells , 2012, Development.

[19]  A. Koltunow,et al.  The Female Gametophyte , 2011, The arabidopsis book.

[20]  David E Hill,et al.  Yeast one-hybrid assays for gene-centered human gene regulatory network mapping , 2011, Nature Methods.

[21]  U. Grossniklaus,et al.  Members of the RKD transcription factor family induce an egg cell-like gene expression program. , 2011, The Plant journal : for cell and molecular biology.

[22]  S. Masiero,et al.  The Emerging Importance of Type I MADS Box Transcription Factors for Plant Reproduction , 2011, Plant Cell.

[23]  Xuemei Chen,et al.  The Anaphase-Promoting Complex Is a Dual Integrator That Regulates Both MicroRNA-Mediated Transcriptional Regulation of Cyclin B1 and Degradation of Cyclin B1 during Arabidopsis Male Gametophyte Development[C][W] , 2011, Plant Cell.

[24]  S. Sprunck,et al.  Nuclear behavior, cell polarity, and cell specification in the female gametophyte , 2011, Sexual Plant Reproduction.

[25]  Ilha Lee,et al.  The FRIGIDA Complex Activates Transcription of FLC, a Strong Flowering Repressor in Arabidopsis, by Recruiting Chromatin Modification Factors[C][W] , 2011, Plant Cell.

[26]  U. Grossniklaus,et al.  VERDANDI Is a Direct Target of the MADS Domain Ovule Identity Complex and Affects Embryo Sac Differentiation in Arabidopsis[W] , 2010, Plant Cell.

[27]  Christian von Mering,et al.  Arabidopsis Female Gametophyte Gene Expression Map Reveals Similarities between Plant and Animal Gametes , 2010, Current Biology.

[28]  K. Shinozaki,et al.  Transduction of RNA‐directed DNA methylation signals to repressive histone marks in Arabidopsis thaliana , 2010, The EMBO journal.

[29]  Xiangfeng Wang,et al.  Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression , 2010, Plant Molecular Biology.

[30]  Shoshi Kikuchi,et al.  Characterization of WRKY co-regulatory networks in rice and Arabidopsis , 2009, BMC Plant Biology.

[31]  Yuehui He Control of the transition to flowering by chromatin modifications. , 2009, Molecular plant.

[32]  Monica Alandete-Saez,et al.  Auxin-Dependent Patterning and Gamete Specification in the Arabidopsis Female Gametophyte , 2009, Science.

[33]  Mikael Bodén,et al.  MEME Suite: tools for motif discovery and searching , 2009, Nucleic Acids Res..

[34]  F. Berger,et al.  The two male gametes share equal ability to fertilize the egg cell in Arabidopsis thaliana , 2009, Current Biology.

[35]  U. Grossniklaus,et al.  CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. , 2008, The Plant journal : for cell and molecular biology.

[36]  M. Menges,et al.  Comprehensive gene expression atlas for the Arabidopsis MAP kinase signalling pathways. , 2008, The New phytologist.

[37]  S. Masiero,et al.  AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[38]  V. Sundaresan,et al.  Cell-Fate Switch of Synergid to Egg Cell in Arabidopsis eostre Mutant Embryo Sacs Arises from Misexpression of the BEL1-Like Homeodomain Gene BLH1[W] , 2007, The Plant Cell Online.

[39]  U. Grossniklaus,et al.  Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte , 2007, Genome Biology.

[40]  Justin O Borevitz,et al.  Genome-Wide Expression Profiling of the Arabidopsis Female Gametophyte Identifies Families of Small, Secreted Proteins , 2007, PLoS genetics.

[41]  Joshua G. Steffen,et al.  Identification of genes expressed in the Arabidopsis female gametophyte. , 2007, The Plant journal : for cell and molecular biology.

[42]  F. Berger,et al.  Distinct Dynamics of HISTONE3 Variants between the Two Fertilization Products in Plants , 2007, Current Biology.

[43]  G. Jürgens,et al.  Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo , 2007, Development.

[44]  G. Jürgens,et al.  LACHESIS Restricts Gametic Cell Fate in the Female Gametophyte of Arabidopsis , 2007, PLoS biology.

[45]  M. Evans The indeterminate gametophyte1 Gene of Maize Encodes a LOB Domain Protein Required for Embryo Sac and Leaf Development[W] , 2007, The Plant Cell Online.

[46]  A. Probst,et al.  Epigenetic regulation of transcription in intermediate heterochromatin , 2006, EMBO reports.

[47]  O. Mathieu,et al.  MOM1 mediates DNA‐methylation‐independent silencing of repetitive sequences in Arabidopsis , 2006, EMBO reports.

[48]  S. Michaels,et al.  SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis , 2006, Development.

[49]  Ilha Lee,et al.  SUPPRESSOR OF FRIGIDA4, Encoding a C2H2-Type Zinc Finger Protein, Represses Flowering by Transcriptional Activation of Arabidopsis FLOWERING LOCUS C[W] , 2006, The Plant Cell Online.

[50]  A. J. Walhout,et al.  Gateway-compatible yeast one-hybrid screens. , 2006, CSH protocols.

[51]  Heping Yang,et al.  EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. , 2006, Planta.

[52]  D. Waugh,et al.  Gateway vectors for the production of combinatorially‐tagged His6‐MBP fusion proteins in the cytoplasm and periplasm of Escherichia coli , 2005, Protein science : a publication of the Protein Society.

[53]  V. Sundaresan,et al.  Analysis of the Female Gametophyte Transcriptome of Arabidopsis by Comparative Expression Profiling1[W] , 2005, Plant Physiology.

[54]  Stefan Scholten,et al.  Construction and screening of subtracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene expression between maize egg cells and central cells. , 2005, The Plant journal : for cell and molecular biology.

[55]  S. Masiero,et al.  ROSINA (RSI), a novel protein with DNA-binding capacity, acts during floral organ development in Antirrhinum majus. , 2005, The Plant journal : for cell and molecular biology.

[56]  P. Langridge,et al.  The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.). , 2005, The Plant journal : for cell and molecular biology.

[57]  Q. Ngo,et al.  Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis , 2005, Development.

[58]  T. Dresselhaus,et al.  Micropylar Pollen Tube Guidance by Egg Apparatus 1 of Maize , 2005, Science.

[59]  Kazuo Shinozaki,et al.  Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoterw⃞ , 2004, The Plant Cell Online.

[60]  R. Yadegari,et al.  Female Gametophyte Development , 2004, The Plant Cell Online.

[61]  R. Amasino,et al.  Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 , 2004, Nature.

[62]  J. T. Kadonaga,et al.  The RNA polymerase II core promoter. , 2003, Annual review of biochemistry.

[63]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[64]  L. Altschmied,et al.  Parthenogenetic egg cells of wheat: cellular and molecular studies , 2001, Sexual Plant Reproduction.

[65]  R. Yadegari,et al.  Mutations in the FIE and MEA Genes That Encode Interacting Polycomb Proteins Cause Parent-of-Origin Effects on Seed Development by Distinct Mechanisms , 2000, Plant Cell.

[66]  L. Aravind The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. , 2000, Trends in biochemical sciences.

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

[68]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[69]  S. Schreiber,et al.  Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex , 1998, Nature.

[70]  G. N. Drews,et al.  Megagametogenesis in Arabidopsis wild type and the Gf mutant , 1997, Sexual Plant Reproduction.

[71]  M. Hülskamp,et al.  Wild‐type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole‐mount tissue , 1995 .

[72]  P. Benfey,et al.  Escholarship@umms Program in Gene Function and Expression Publications and Presentations Program in Gene Function and Expression a Stele-enriched Gene Regulatory Network in the Arabidopsis Root Repository Citation a Stele-enriched Gene Regulatory Network in the Arabidopsis Root a Stele-enriched Gene , 2022 .

[73]  Toshiro Ito,et al.  Functional roles of histone modification, chromatin remodeling and microRNAs in Arabidopsis flower development. , 2013, International review of cell and molecular biology.

[74]  S. Lopato,et al.  Isolation of plant transcription factors using a modified yeast one-hybrid system , 2006, Plant Methods.

[75]  BMC Genomics BioMed Central Research article , 2005 .

[76]  K. Shinozaki,et al.  Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoter , 2004 .

[77]  C. Lister,et al.  Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN 3 , 2022 .

[78]  V. Sundaresan,et al.  Supplemental Information The CKI 1 Histidine Kinase Speci fi es the Female Gametic Precursor of the Endosperm , 2022 .