HISTONE DEACETYLASE19 Interacts with HSL1 and Participates in the Repression of Seed Maturation Genes in Arabidopsis Seedlings[C][W]

HDA19 interacts with HSL1 and together they negatively regulate seed maturation gene expression in vegetative organs, suggesting that epigenetic regulation is critical for seed development. This study provides insight into the molecular mechanism underlying the gene regulation in seed development. The seed maturation genes are specifically and highly expressed during late embryogenesis. In this work, yeast two-hybrid, bimolecular fluorescence complementation, and coimmunoprecipitation assays revealed that HISTONE DEACETYLASE19 (HDA19) interacted with the HIGH-LEVEL EXPRESSION OF SUGAR-INDUCIBLE GENE2-LIKE1 (HSL1), and the zinc-finger CW [conserved Cys (C) and Trp (W) residues] domain of HSL1 was responsible for the interaction. Furthermore, we found that mutations in HDA19 resulted in the ectopic expression of seed maturation genes in seedlings, which was associated with increased levels of gene activation marks, such as Histone H3 acetylation (H3ac), Histone H4 acetylation (H4ac), and Histone H3 Lys 4 tri-methylation (H3K4me3), but decreased levels of the gene repression mark Histone H3 Lys 27 tri-methylation (H3K27me3) in the promoter and/or coding regions. In addition, elevated transcription of certain seed maturation genes was also found in the hsl1 mutant seedlings, which was also accompanied by the enrichment of gene activation marks but decreased levels of the gene repression mark. Chromatin immunoprecipitation assays showed that HDA19 could directly bind to the chromatin of the seed maturation genes. These results suggest that HDA19 and HSL1 may act together to repress seed maturation gene expression during germination. Further genetic analyses revealed that the homozygous hsl1 hda19 double mutants are embryonic lethal, suggesting that HDA19 and HSL1 may play a vital role during embryogenesis.

[1]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[2]  Xuncheng Liu,et al.  Histone Deacetylase HDA6 Is Functionally Associated with AS1 in Repression of KNOX Genes in Arabidopsis , 2012, PLoS Genetics.

[3]  Xuemei Chen,et al.  MicroRNA–Mediated Repression of the Seed Maturation Program during Vegetative Development in Arabidopsis , 2012, PLoS genetics.

[4]  W. Keller,et al.  Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings , 2011, Journal of experimental botany.

[5]  Yuhai Cui,et al.  Detection of protein interactions in plant using a gateway compatible bimolecular fluorescence complementation (BiFC) system. , 2011, Journal of visualized experiments : JoVE.

[6]  T. Jenuwein,et al.  Arabidopsis REF6 is a histone H3 lysine 27 demethylase , 2011, Nature Genetics.

[7]  Rein Aasland,et al.  The CW domain, a new histone recognition module in chromatin proteins , 2011, The EMBO journal.

[8]  Xuncheng Liu,et al.  HISTONE DEACETYLASE6 Interacts with FLOWERING LOCUS D and Regulates Flowering in Arabidopsis1[C][W][OA] , 2011, Plant Physiology.

[9]  Arp Schnittger,et al.  Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition , 2011, PLoS genetics.

[10]  N. Chua,et al.  Rapid and Reversible Light-Mediated Chromatin Modifications of Arabidopsis Phytochrome A Locus[C][W] , 2011, Plant Cell.

[11]  T. Umehara,et al.  Structural insight into the zinc finger CW domain as a histone modification reader. , 2010, Structure.

[12]  M. Seki,et al.  Chromatin regulation functions in plant abiotic stress responses. , 2010, Plant, cell & environment.

[13]  Keqiang Wu,et al.  Epigenetic regulation of peanut allergen gene Ara h 3 in developing embryos , 2010, Planta.

[14]  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.

[15]  Tommy S. Jørstad,et al.  The ASH1 HOMOLOG 2 (ASHH2) Histone H3 Methyltransferase Is Required for Ovule and Anther Development in Arabidopsis , 2009, PloS one.

[16]  W. Keller,et al.  Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. , 2009, The Plant journal : for cell and molecular biology.

[17]  Keqiang Wu,et al.  Regulation of oleosin expression in developing peanut (Arachis hypogaea L.) embryos through nucleosome loss and histone modifications. , 2009, Journal of experimental botany.

[18]  D. Meinke,et al.  Integrating the Genetic and Physical Maps of Arabidopsis thaliana: Identification of Mapped Alleles of Cloned Essential (EMB) Genes , 2009, PloS one.

[19]  M. Motto,et al.  Chromatin and DNA Modifications in the Opaque2-Mediated Regulation of Gene Transcription during Maize Endosperm Development[W] , 2009, The Plant Cell Online.

[20]  F. Forneris,et al.  A Novel Mammalian Flavin-dependent Histone Demethylase* , 2009, The Journal of Biological Chemistry.

[21]  Xiang Li,et al.  Repression of Seed Maturation Genes by a Trihelix Transcriptional Repressor in Arabidopsis Seedlings[W] , 2009, The Plant Cell Online.

[22]  Masaharu Suzuki,et al.  Functional symmetry of the B3 network controlling seed development. , 2008, Current opinion in plant biology.

[23]  N. Chua,et al.  betaC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. , 2008, Genes & development.

[24]  Kang-Chang Kim,et al.  Arabidopsis WRKY38 and WRKY62 Transcription Factors Interact with Histone Deacetylase 19 in Basal Defense[W] , 2008, The Plant Cell Online.

[25]  W. Keller,et al.  The Arabidopsis BRAHMA Chromatin-Remodeling ATPase Is Involved in Repression of Seed Maturation Genes in Leaves1[W][OA] , 2008, Plant Physiology.

[26]  Keqiang Wu,et al.  HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. , 2008, Journal of experimental botany.

[27]  L. Lopez-Molina,et al.  The role of chromatin-remodeling factor PKL in balancing osmotic stress responses during Arabidopsis seed germination. , 2007, The Plant journal : for cell and molecular biology.

[28]  D. Wagner,et al.  Histone modifications and dynamic regulation of genome accessibility in plants. , 2007, Current opinion in plant biology.

[29]  H. Kamada,et al.  The Arabidopsis Histone Deacetylases HDA6 and HDA19 Contribute to the Repression of Embryonic Properties after Germination1[W] , 2007, Plant Physiology.

[30]  R. Amasino,et al.  Arabidopsis Relatives of the Human Lysine-Specific Demethylase1 Repress the Expression of FWA and FLOWERING LOCUS C and Thus Promote the Floral Transition[W] , 2007, The Plant Cell Online.

[31]  J. Sheen,et al.  Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis , 2007, Nature Protocols.

[32]  Matteo Pellegrini,et al.  Whole-Genome Analysis of Histone H3 Lysine 27 Trimethylation in Arabidopsis , 2007, PLoS biology.

[33]  Hironaka Tsukagoshi,et al.  Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings , 2007, Proceedings of the National Academy of Sciences.

[34]  Masaharu Suzuki,et al.  Repression of the LEAFY COTYLEDON 1/B3 Regulatory Network in Plant Embryo Development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 Genes1[C][W] , 2006, Plant Physiology.

[35]  X. Deng.  Faculty Opinions recommendation of Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. , 2006 .

[36]  C. Hawes,et al.  Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants , 2006, Nature Protocols.

[37]  Daoxiu Zhou,et al.  Arabidopsis GCN5, HD1, and TAF1/HAF2 Interact to Regulate Histone Acetylation Required for Light-Responsive Gene Expression , 2006, The Plant Cell Online.

[38]  U. Grossniklaus,et al.  Different Polycomb group complexes regulate common target genes in Arabidopsis , 2006, EMBO reports.

[39]  P. Ronald,et al.  A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts , 2006, Plant Methods.

[40]  Z. Chen,et al.  Arabidopsis thaliana histone deacetylase 1 (AtHD1) is localized in euchromatic regions and demonstrates histone deacetylase activity in vitro , 2006, Cell Research.

[41]  Robert B Goldberg,et al.  Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Hall,et al.  Ordered Histone Modifications Are Associated with Transcriptional Poising and Activation of the phaseolin Promoter , 2005, The Plant Cell Online.

[43]  T. Beardmore,et al.  Dynamic Histone Acetylation of Late Embryonic Genes during Seed Germination , 2005, Plant Molecular Biology.

[44]  W. Shen,et al.  Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36 , 2005, Nature Cell Biology.

[45]  S. D. Rider,et al.  PICKLE acts during germination to repress expression of embryonic traits. , 2005, The Plant journal : for cell and molecular biology.

[46]  L. Lepiniec,et al.  LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves , 2005, FEBS letters.

[47]  D. Shibata,et al.  Analysis of a Sugar Response Mutant of Arabidopsis Identified a Novel B3 Domain Protein That Functions as an Active Transcriptional Repressor1 , 2005, Plant Physiology.

[48]  Keqiang Wu,et al.  HISTONE DEACETYLASE19 Is Involved in Jasmonic Acid and Ethylene Signaling of Pathogen Response in Arabidopsis , 2005, The Plant Cell Online.

[49]  Xiang-Jiao Yang,et al.  Class II Histone Deacetylases: from Sequence to Function, Regulation, and Clinical Implication , 2005, Molecular and Cellular Biology.

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

[51]  Yang Shi,et al.  Histone Demethylation Mediated by the Nuclear Amine Oxidase Homolog LSD1 , 2004, Cell.

[52]  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.

[53]  Masanori Okamoto,et al.  The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. , 2004, Developmental cell.

[54]  S. D. Rider,et al.  Metabolic profiling of the Arabidopsis pkl mutant reveals selective derepression of embryonic traits , 2004, Planta.

[55]  S. D. Rider,et al.  PICKLE Acts throughout the Plant to Repress Expression of Embryonic Traits and May Play a Role in Gibberellin-Dependent Responses1 , 2004, Plant Physiology.

[56]  G. Felsenfeld,et al.  Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9 , 2004, The EMBO journal.

[57]  Yunde Zhao,et al.  The CW domain, a structural module shared amongst vertebrates, vertebrate-infecting parasites and higher plants. , 2003, Trends in biochemical sciences.

[58]  Kevin Struhl,et al.  The Rtf1 Component of the Paf1 Transcriptional Elongation Complex Is Required for Ubiquitination of Histone H2B* , 2003, Journal of Biological Chemistry.

[59]  Z. Chen,et al.  Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. , 2003, Genetics.

[60]  H. Edenberg,et al.  Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[61]  U. Grossniklaus,et al.  Epigenetic inheritance of expression states in plant development: the role of Polycomb group proteins. , 2002, Current opinion in cell biology.

[62]  L. Lepiniec,et al.  LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[63]  C. Allis,et al.  Correlation Between Histone Lysine Methylation and Developmental Changes at the Chicken β-Globin Locus , 2001, Science.

[64]  K. Hiratsu,et al.  Repression Domains of Class II ERF Transcriptional Repressors Share an Essential Motif for Active Repression , 2001, The Plant Cell Online.

[65]  C. Allis,et al.  Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[66]  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.

[67]  P. Herrmann,et al.  FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[68]  Robert B Goldberg,et al.  Arabidopsis LEAFY COTYLEDON1 Is Sufficient to Induce Embryo Development in Vegetative Cells , 1998, Cell.

[69]  C. Somerville,et al.  Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. , 1997, Science.

[70]  T. Laux,et al.  Embryogenesis: A New Start in Life. , 1997, The Plant cell.

[71]  F. Parcy,et al.  Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. , 1994, The Plant cell.

[72]  R. Yadegari,et al.  Plant Embryogenesis: Zygote to Seed , 1994, Science.

[73]  H. Goodman,et al.  Isolation of the Arabidopsis ABI3 gene by positional cloning. , 1992, The Plant cell.

[74]  Yuanyuan Li,et al.  Many keys to push: diversifying the 'readership' of plant homeodomain fingers. , 2012, Acta biochimica et biophysica Sinica.

[75]  Jesús Vicente-Carbajosa,et al.  Seed maturation: developing an intrusive phase to accomplish a quiescent state. , 2005, The International journal of developmental biology.

[76]  K. Struhl,et al.  The Rtf 1 Component of the Paf 1 Transcriptional Elongation Complex Is Required for Ubiquitination of Histone H 2 B * , 2003 .

[77]  J. Harada.  Role of Arabidopsis LEAFY COTYLEDON genes in seed development , 2001 .

[78]  P. Herrmann,et al.  FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.