Histone Deacetylase Complex1 Expression Level Titrates Plant Growth and Abscisic Acid Sensitivity in Arabidopsis[C][W][OPEN]

Chemical modification of histones alters DNA structure and regulates gene expression. We have identified the Histone Deacetylase Complex (HDC) 1 protein as a component of chromatin in plants required for histone deacetylation and for induction of stress-inducible genes. HDC1-overexpression improves germination and plant growth without affecting plant morphology. Histone deacetylation regulates gene expression during plant stress responses and is therefore an interesting target for epigenetic manipulation of stress sensitivity in plants. Unfortunately, overexpression of the core enzymes (histone deacetylases [HDACs]) has either been ineffective or has caused pleiotropic morphological abnormalities. In yeast and mammals, HDACs operate within multiprotein complexes. Searching for putative components of plant HDAC complexes, we identified a gene with partial homology to a functionally uncharacterized member of the yeast complex, which we called Histone Deacetylation Complex1 (HDC1). HDC1 is encoded by a single-copy gene in the genomes of model plants and crops and therefore presents an attractive target for biotechnology. Here, we present a functional characterization of HDC1 in Arabidopsis thaliana. We show that HDC1 is a ubiquitously expressed nuclear protein that interacts with at least two deacetylases (HDA6 and HDA19), promotes histone deacetylation, and attenuates derepression of genes under water stress. The fast-growing HDC1-overexpressing plants outperformed wild-type plants not only on well-watered soil but also when water supply was reduced. Our findings identify HDC1 as a rate-limiting component of the histone deacetylation machinery and as an attractive tool for increasing germination rate and biomass production of plants.

[1]  V. Colot,et al.  Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome , 2013, Genome Biology.

[2]  Zhongchi Liu,et al.  Histone deacetylase genes in Arabidopsis development. , 2008, Journal of integrative plant biology.

[3]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[4]  Christopher Grefen,et al.  A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). , 2012, BioTechniques.

[5]  A. Daszkowska-Golec,et al.  Arabidopsis seed germination under abiotic stress as a concert of action of phytohormones. , 2011, Omics : a journal of integrative biology.

[6]  C. Koncz,et al.  The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector , 1986, Molecular and General Genetics MGG.

[7]  Keqiang Wu,et al.  Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response , 2010, Journal of experimental botany.

[8]  K. Shinozaki,et al.  Arabidopsis HDA6 Regulates Locus-Directed Heterochromatin Silencing in Cooperation with MET1 , 2011, PLoS genetics.

[9]  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.

[10]  T. Kouzarides Chromatin Modifications and Their Function , 2007, Cell.

[11]  V. Colot,et al.  Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. , 2009, Trends in genetics : TIG.

[12]  J. Micol,et al.  Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress. , 2006, Plant, cell & environment.

[13]  Wei Li,et al.  Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[14]  Michael Grunstein,et al.  Histone acetylation and deacetylation in yeast , 2003, Nature Reviews Molecular Cell Biology.

[15]  S. Berger The complex language of chromatin regulation during transcription , 2007, Nature.

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

[17]  C. Steber,et al.  Molecular aspects of seed dormancy. , 2008, Annual review of plant biology.

[18]  Michael P Washburn,et al.  Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. , 2005, Biochimica et biophysica acta.

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

[20]  Zhi-hong Xu,et al.  Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Richa Agarwala,et al.  COBALT: constraint-based alignment tool for multiple protein sequences , 2007, Bioinform..

[22]  M. Van Montagu,et al.  Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco , 2011, Proceedings of the National Academy of Sciences.

[23]  Jian-Kang Zhu,et al.  Role of an Arabidopsis AP2/EREBP-Type Transcriptional Repressor in Abscisic Acid and Drought Stress Responses , 2005, The Plant Cell Online.

[24]  Fabian Kellermeier,et al.  Natural Variation of Arabidopsis Root Architecture Reveals Complementing Adaptive Strategies to Potassium Starvation1[C][W][OA] , 2013, Plant Physiology.

[25]  N. Krogan,et al.  SIN-fully silent: HDAC complexes in fission yeast , 2007, Nature Structural &Molecular Biology.

[26]  K. Chenu,et al.  PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. , 2006, The New phytologist.

[27]  Keqiang Wu,et al.  Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response , 2010, Plant signaling & behavior.

[28]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[29]  D. Galbraith,et al.  AtSAP18, An Orthologue of Human SAP18, is Involved in the Regulation of Salt Stress and Mediates Transcriptional Repression in Arabidopsis , 2005, Plant Molecular Biology.

[30]  Xuncheng Liu,et al.  HDA 6 Directly Interacts with DNA Methyltransferase MET 1 and Maintains Transposable Element Silencing in Arabidopsis 1 [ W ] [ OA ] , 2011 .

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

[32]  H. Bohnert,et al.  Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance , 2008, Proceedings of the National Academy of Sciences.

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

[34]  Z. Chen,et al.  Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Grunstein,et al.  The Rpd3 Core Complex Is a Chromatin Stabilization Module , 2012, Current Biology.

[36]  Y. Sakata,et al.  ABA in bryophytes: how a universal growth regulator in life became a plant hormone? , 2011, Journal of Plant Research.

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

[38]  M. Blatt,et al.  The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain. , 2002, The Plant cell.

[39]  E. Bornberg-Bauer,et al.  The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. , 2007, The Plant journal : for cell and molecular biology.

[40]  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.

[41]  M. Motto,et al.  Maize Histone Deacetylase hda101 Is Involved in Plant Development, Gene Transcription, and Sequence-Specific Modulation of Histone Modification of Genes and Repeats[W] , 2007, The Plant Cell Online.

[42]  J. Kudla,et al.  A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. , 2010, The Plant journal : for cell and molecular biology.

[43]  A. Amtmann,et al.  Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. , 2006, Journal of experimental botany.

[44]  Bing Li,et al.  Histone H3 Methylation by Set2 Directs Deacetylation of Coding Regions by Rpd3S to Suppress Spurious Intragenic Transcription , 2005, Cell.

[45]  S. Michaels,et al.  Arabidopsis Homologs of Retinoblastoma-Associated Protein 46/48 Associate with a Histone Deacetylase to Act Redundantly in Chromatin Silencing , 2011, PLoS genetics.

[46]  U. Grossniklaus,et al.  Selected aspects of transgenerational epigenetic inheritance and resetting in plants. , 2011, Current opinion in plant biology.

[47]  I. Ladunga,et al.  The Highly Similar Arabidopsis Homologs of Trithorax ATX1 and ATX2 Encode Proteins with Divergent Biochemical Functions[W] , 2008, The Plant Cell Online.

[48]  Xuncheng Liu,et al.  HDA6 Directly Interacts with DNA Methyltransferase MET1 and Maintains Transposable Element Silencing in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[49]  C. Tonelli,et al.  Survival and growth of Arabidopsis plants given limited water are not equal , 2011, Nature Biotechnology.

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

[51]  P. Mourrain,et al.  Arabidopsis Histone Deacetylase HDA6 Is Required for Maintenance of Transcriptional Gene Silencing and Determines Nuclear Organization of rDNA Repeats , 2004, The Plant Cell Online.

[52]  M. Seki,et al.  An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by histone deacetylase 6. , 2012, Plant & cell physiology.

[53]  K. Paszkiewicz,et al.  The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. , 2012, Plant, cell & environment.

[54]  H. Kwon,et al.  Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. , 2003, The Plant journal : for cell and molecular biology.

[55]  D. Baulcombe,et al.  An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. , 2003, The Plant journal : for cell and molecular biology.

[56]  U. Grossniklaus,et al.  A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta[w] , 2003, Plant Physiology.

[57]  E. Seto,et al.  The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men , 2008, Nature Reviews Molecular Cell Biology.