Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination.

The transition between dormancy and germination represents a critical stage in the life cycle of higher plants and is an important ecological and commercial trait. In this review we present current knowledge of the molecular control of this trait in Arabidopsis thaliana, focussing on important components functioning during the developmental phases of seed maturation, after-ripening and imbibition. Establishment of dormancy during seed maturation is regulated by networks of transcription factors with overlapping and discrete functions. Following desiccation, after-ripening determines germination potential and, surprisingly, recent observations suggest that transcriptional and post-transcriptional processes occur in the dry seed. The single-cell endosperm layer that surrounds the embryo plays a crucial role in the maintenance of dormancy, and transcriptomics approaches are beginning to uncover endosperm-specific genes and processes. Molecular genetic approaches have provided many new components of hormone signalling pathways, but also indicate the importance of hormone-independent pathways and of natural variation in key regulatory loci. The influence of environmental signals (particularly light) following after-ripening, and the effect of moist chilling (stratification) are increasingly being understood at the molecular level. Combined postgenomics, physiology and molecular genetics approaches are beginning to provide an unparalleled understanding of the molecular processes underlying dormancy and germination.

[1]  D. Weiss,et al.  Mechanisms of Cross Talk between Gibberellin and Other Hormones1 , 2007, Plant Physiology.

[2]  C. Baskin,et al.  A classification system for seed dormancy , 2004, Seed Science Research.

[3]  C. Almoguera,et al.  Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs , 1992, Plant Molecular Biology.

[4]  C. Kao,et al.  Cooperative DNA Binding Activity , 1997 .

[5]  R. Quatrano,et al.  A Conserved Domain of the viviparous-1 Gene Product Enhances the DNA Binding Activity of the bZIP Protein EmBP-1 and Other Transcription Factors (*) , 1996, The Journal of Biological Chemistry.

[6]  M. Koornneef,et al.  Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. , 2000, Plant physiology.

[7]  S. Tabata,et al.  Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. , 2006, The Plant journal : for cell and molecular biology.

[8]  J. Vandekerckhove,et al.  The Effect of α-Amanitin on the Arabidopsis Seed Proteome Highlights the Distinct Roles of Stored and Neosynthesized mRNAs during Germination1 , 2004, Plant Physiology.

[9]  S. Kurup,et al.  The Arabidopsis COMATOSE locus regulates germination potential. , 2000, Development.

[10]  L. Hennig,et al.  The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. , 2003, Genes & development.

[11]  U. Wobus,et al.  The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis , 1994 .

[12]  J. Bewley,et al.  Seed Germination and Dormancy. , 1997, The Plant cell.

[13]  T. Wohlfarth,et al.  Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. , 2000, The Plant journal : for cell and molecular biology.

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

[15]  J. Giraudat,et al.  Interactions between Abscisic Acid and Ethylene Signaling Cascades , 2000, Plant Cell.

[16]  L. Lopez-Molina,et al.  A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  P. Busk,et al.  Regulation of abscisic acid-induced transcription , 1998, Plant Molecular Biology.

[18]  G. Storz,et al.  Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. , 1995, The Plant journal : for cell and molecular biology.

[19]  Jinrong Peng,et al.  Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. , 2002, Genes & development.

[20]  M. Holdsworth,et al.  Use of comparative molecular genetics to study pre harvest sprouting in wheat , 2002, Euphytica.

[21]  Yuji Kamiya,et al.  Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. , 2005, The Plant journal : for cell and molecular biology.

[22]  S. Iuchi,et al.  Identification and characterization of Arabidopsis gibberellin receptors. , 2006, The Plant journal : for cell and molecular biology.

[23]  K. Struhl,et al.  Targeted Recruitment of the Sin3-Rpd3 Histone Deacetylase Complex Generates a Highly Localized Domain of Repressed Chromatin In Vivo , 1998, Molecular and Cellular Biology.

[24]  S. J. Ambrose,et al.  The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. , 2005, The Plant journal : for cell and molecular biology.

[25]  Eiji Nambara,et al.  ABA action and interactions in seeds. , 2003, Trends in plant science.

[26]  Noah Fahlgren,et al.  Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. , 2007, The Plant journal : for cell and molecular biology.

[27]  K. Halliday,et al.  DELLA-Mediated Cotyledon Expansion Breaks Coat-Imposed Seed Dormancy , 2006, Current Biology.

[28]  F. Apone,et al.  GCR1, the putative Arabidopsis G protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  P. Verslues,et al.  Identification of Two Protein Kinases Required for Abscisic Acid Regulation of Seed Germination, Root Growth, and Gene Expression in Arabidopsis[W] , 2007, The Plant Cell Online.

[30]  T. Schmülling,et al.  Arabidopsis Cytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism[W] , 2005, The Plant Cell Online.

[31]  Diana V. Dugas,et al.  MicroRNA regulation of gene expression in plants. , 2004, Current opinion in plant biology.

[32]  Robert B Goldberg,et al.  LEAFY COTYLEDON1-LIKE Defines a Class of Regulators Essential for Embryo Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006973. , 2003, The Plant Cell Online.

[33]  Michael J Holdsworth,et al.  Gene Expression Profiling Reveals Defined Functions of the ATP-Binding Cassette Transporter COMATOSE Late in Phase II of Germination1[W][OA] , 2007, Plant Physiology.

[34]  V. Germain,et al.  Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Y. Kamiya,et al.  CYP707A1 and CYP707A2, Which Encode Abscisic Acid 8′-Hydroxylases, Are Indispensable for Proper Control of Seed Dormancy and Germination in Arabidopsis1 , 2006, Plant Physiology.

[36]  Nam-Hai Chua,et al.  ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. , 2002, The Plant journal : for cell and molecular biology.

[37]  D. Ohta,et al.  Arabidopsis CYP707As Encode (+)-Abscisic Acid 8′-Hydroxylase, a Key Enzyme in the Oxidative Catabolism of Abscisic Acid1 , 2004, Plant Physiology.

[38]  Nam-Hai Chua,et al.  ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. , 2007, The Plant journal : for cell and molecular biology.

[39]  L. Lepiniec,et al.  The Arabidopsis AtEPR1 extensin-like gene is specifically expressed in endosperm during seed germination. , 2000, The Plant journal : for cell and molecular biology.

[40]  C. Bailly,et al.  ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. , 2007, The Plant journal : for cell and molecular biology.

[41]  T. Lynch,et al.  The Arabidopsis Abscisic Acid Response Gene ABI5 Encodes a Basic Leucine Zipper Transcription Factor , 2000, Plant Cell.

[42]  Alan M. Jones,et al.  Role of a Heterotrimeric G Protein in Regulation of Arabidopsis Seed Germination1 , 2002, Plant Physiology.

[43]  Q. Shen,et al.  Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. , 1996, The Plant cell.

[44]  Michael J Holdsworth,et al.  Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis , 2007, The Plant journal : for cell and molecular biology.

[45]  C. M. Karssen,et al.  Dormancy and Germination of Abscisic Acid-Deficient Tomato Seeds : Studies with the sitiens Mutant. , 1992, Plant physiology.

[46]  M. Wagner,et al.  Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana , 2004, Planta.

[47]  Eunkyoo Oh,et al.  PIL5, a Phytochrome-Interacting bHLH Protein, Regulates Gibberellin Responsiveness by Binding Directly to the GAI and RGA Promoters in Arabidopsis Seeds[W] , 2007, The Plant Cell Online.

[48]  P. McCourt,et al.  Hormone Cross-Talk in Seed Dormancy , 2003, Journal of Plant Growth Regulation.

[49]  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.

[50]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010441. , 2002, The Plant Cell Online.

[51]  M. Grunstein,et al.  Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3 , 1998, Nature.

[52]  F. Parcy,et al.  Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. , 1997, The Plant journal : for cell and molecular biology.

[53]  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.

[54]  M. Koornneef,et al.  Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. , 2000, Plant physiology.

[55]  G. Leubner-Metzger,et al.  beta-1,3-Glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. , 2004, The Plant journal : for cell and molecular biology.

[56]  J. Vandekerckhove,et al.  Proteomic analysis of arabidopsis seed germination and priming. , 2001, Plant physiology.

[57]  P. McCourt,et al.  Regulation of Abscisic Acid Signaling by the Ethylene Response Pathway in Arabidopsis , 2000, Plant Cell.

[58]  L. Lopez-Molina,et al.  AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. , 2003, Genes & development.

[59]  C. Steber,et al.  Seed Germination of GA-Insensitive sleepy1 Mutants Does Not Require RGL2 Protein Disappearance in Arabidopsis[W] , 2007, The Plant Cell Online.

[60]  C. Job,et al.  Patterns of Protein Oxidation in Arabidopsis Seeds and during Germination1[w] , 2005, Plant Physiology.

[61]  P. Christou,et al.  ‘Green revolution’ genes encode mutant gibberellin response modulators , 1999, Nature.

[62]  C. M. Karssen,et al.  The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh. , 1982, Theoretical and Applied Genetics.

[63]  K. Bradford,et al.  A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. , 2002, Journal of experimental botany.

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

[65]  Eunkyoo Oh,et al.  PIL5, a Phytochrome-Interacting Basic Helix-Loop-Helix Protein, Is a Key Negative Regulator of Seed Germination in Arabidopsis thalianaw⃞ , 2004, The Plant Cell Online.

[66]  D. Inzé,et al.  The Role of the Cell Cycle Machinery in Resumption of Postembryonic Development1 , 2005, Plant Physiology.

[67]  T. Minamikawa,et al.  Stored mRNA in cotyledons of Vigna unguiculata seeds: nucleotide sequence of cloned cDNA for a stored mRNA and induction of its synthesis by precocious germination , 1990, Plant Molecular Biology.

[68]  Y. Kamiya,et al.  Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[69]  Maarten Koornneef,et al.  A gibberellin insensitive mutant of Arabidopsis thaliana , 1985 .

[70]  W. Finch-Savage,et al.  Seed dormancy and the control of germination. , 2006, The New phytologist.

[71]  J. Vandekerckhove,et al.  Proteomics of Arabidopsis seed germination and priming. , 2003 .

[72]  I. Ezcurra,et al.  Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription , 1996, Plant Molecular Biology.

[73]  E. Grill,et al.  Relay and control of abscisic acid signaling. , 2003, Current opinion in plant biology.

[74]  M. Koornneef,et al.  Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. , 2003, Genetics.

[75]  M. Delseny,et al.  Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L. , 2000, Journal of experimental botany.

[76]  Ramón Serrano,et al.  Enhancement of Abscisic Acid Sensitivity and Reduction of Water Consumption in Arabidopsis by Combined Inactivation of the Protein Phosphatases Type 2C ABI1 and HAB11[W] , 2006, Plant Physiology.

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

[78]  J. Bowman,et al.  Distinct Mechanisms Promote Polarity Establishment in Carpels of Arabidopsis , 1999, Cell.

[79]  K. Thompson,et al.  Seeds: Physiology of Development and Germination , 1986 .

[80]  C. Schwechheimer,et al.  The DELLA Domain of GA INSENSITIVE Mediates the Interaction with the GA INSENSITIVE DWARF1A Gibberellin Receptor of Arabidopsis[W] , 2007, The Plant Cell Online.

[81]  WangLJ Auxin distribution and transport during embryogenesis and seed germination of Arabidopsis , 2001 .

[82]  Alan M. Jones,et al.  Comment on "A G Protein–Coupled Receptor Is a Plasma Membrane Receptor for the Plant Hormone Abscisic Acid" , 2007, Science.

[83]  J. Vandekerckhove,et al.  Proteomics of Arabidopsis Seed Germination. A Comparative Study of Wild-Type and Gibberellin-Deficient Seeds1 , 2002, Plant Physiology.

[84]  Zhong-Lin Zhang,et al.  Genetic Characterization and Functional Analysis of the GID1 Gibberellin Receptors in Arabidopsis[W] , 2006, The Plant Cell Online.

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

[86]  Philippe Lucas,et al.  Gene expression analysis by cDNA-AFLP highlights a set of new signaling networks and translational control during seed dormancy breaking in Nicotiana plumbaginifolia , 2005, Plant Molecular Biology.

[87]  R R Finkelstein,et al.  Physical interactions between ABA response loci of Arabidopsis. , 2001, The Plant journal : for cell and molecular biology.

[88]  M. Holdsworth,et al.  Jasmonic Acid Levels Are Reduced in COMATOSE ATP-Binding Cassette Transporter Mutants. Implications for Transport of Jasmonate Precursors into Peroxisomes1 , 2005, Plant Physiology.

[89]  L. Dure,et al.  Long-Lived Messenger RNA: Evidence from Cotton Seed Germination , 1965, Science.

[90]  D. W. Hughes,et al.  Temporally modular gene expression during cotyledon development. , 1989, Genes & development.

[91]  G. Bassel,et al.  Down-Regulation of DELLA Genes Is Not Essential for Germination of Tomato, Soybean, and Arabidopsis Seeds1 , 2004, Plant Physiology.

[92]  K. Shinozaki,et al.  Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. , 2004, Plant & cell physiology.

[93]  M. Holdsworth,et al.  Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. , 2000, The Plant journal : for cell and molecular biology.

[94]  A. Jermakow,et al.  Gibberellins Are Required for Seed Development and Pollen Tube Growth in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003046. , 2002, The Plant Cell Online.

[95]  U. Wobus,et al.  Sugars as Signal Molecules in Plant Seed Development , 1999, Biological chemistry.

[96]  Po-Pu Liu,et al.  The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. , 2005, The Plant journal : for cell and molecular biology.

[97]  J. Schroeder,et al.  An mRNA Cap Binding Protein, ABH1, Modulates Early Abscisic Acid Signal Transduction in Arabidopsis , 2001, Cell.

[98]  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.

[99]  R. Hill,et al.  The RNA-binding protein FCA is an abscisic acid receptor , 2006, Nature.

[100]  E. Nambara,et al.  Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. , 2006, The Plant journal : for cell and molecular biology.

[101]  B. Ellis,et al.  Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[102]  Y. Kamiya,et al.  The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′‐hydroxylases: key enzymes in ABA catabolism , 2004, The EMBO journal.

[103]  Gerhard Leubner-Metzger,et al.  Plant hormone interactions during seed dormancy release and germination , 2005, Seed Science Research.

[104]  I. Díaz,et al.  Synergistic Activation of Seed Storage Protein Gene Expression in Arabidopsis by ABI3 and Two bZIPs Related to OPAQUE2* , 2003, Journal of Biological Chemistry.

[105]  Alexandra To,et al.  A Network of Local and Redundant Gene Regulation Governs Arabidopsis Seed Maturation , 2006, The Plant Cell Online.

[106]  Kamel Chibani,et al.  Proteomic Analysis of Seed Dormancy in Arabidopsis1[W] , 2006, Plant Physiology.

[107]  M. Holdsworth,et al.  Chewing the fat: beta-oxidation in signalling and development. , 2006, Trends in plant science.

[108]  Yuji Kamiya,et al.  Activation of Gibberellin Biosynthesis and Response Pathways by Low Temperature during Imbibition of Arabidopsis thaliana Seeds On-line version contains Web-only data. , 2004, The Plant Cell Online.

[109]  Russell L. Jones,et al.  The Arabidopsis Aleurone Layer Responds to Nitric Oxide, Gibberellin, and Abscisic Acid and Is Sufficient and Necessary for Seed Dormancy1[C][W][OA] , 2007, Plant Physiology.

[110]  P. Toorop,et al.  Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. , 2006, The Plant journal : for cell and molecular biology.

[111]  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.

[112]  C. Rock,et al.  Tansley Review No. 120: Pathways to abscisic acid-regulated gene expression. , 2000, The New phytologist.

[113]  K. Roberts,et al.  AtAGP30, an arabinogalactan-protein in the cell walls of the primary root, plays a role in root regeneration and seed germination. , 2003, The Plant journal : for cell and molecular biology.

[114]  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.

[115]  Wei-Hua Wu,et al.  A G Protein-Coupled Receptor Is a Plasma Membrane Receptor for the Plant Hormone Abscisic Acid , 2007, Science.

[116]  C. M. Karssen,et al.  Acquisition of Desiccation Tolerance and Longevity in Seeds of Arabidopsis thaliana (A Comparative Study Using Abscisic Acid-Insensitive abi3 Mutants) , 1993, Plant physiology.

[117]  N. Chua,et al.  The AIP 2 E 3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI 3 degradation , 2005 .

[118]  C. D. Dickinson,et al.  RY repeats are conserved in the 5'-flanking regions of legume seed- protein genes , 1988, Nucleic Acids Res..

[119]  Steven Penfield,et al.  Reserve Mobilization in the Arabidopsis Endosperm Fuels Hypocotyl Elongation in the Dark, Is Independent of Abscisic Acid, and Requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1 , 2004, The Plant Cell Online.

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

[121]  C. M. Karssen,et al.  The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana , 1984 .

[122]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[123]  M. Holdsworth,et al.  Chewing the fat: beta-oxidation in signalling and development. , 2006, Trends in plant science.

[124]  A. Kermode,et al.  An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. , 2000, Plant physiology.

[125]  E. Golovina,et al.  Mechanisms of plant desiccation tolerance. , 2001, Trends in plant science.

[126]  M. Koornneef,et al.  Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis , 2006, Proceedings of the National Academy of Sciences.

[127]  Jianhua Zhang,et al.  The Regulator of G-Protein Signaling Proteins Involved in Sugar and Abscisic Acid Signaling in Arabidopsis Seed Germination1 , 2005, Plant Physiology.

[128]  F. Parcy,et al.  AtGA3ox2, a Key Gene Responsible for Bioactive Gibberellin Biosynthesis, Is Regulated during Embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis1 , 2004, Plant Physiology.

[129]  D. Galbraith,et al.  Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. , 2001, Developmental cell.

[130]  L. Comai,et al.  Transcriptional activities in dry seed nuclei indicate the timing of the transition from embryogeny to germination. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[131]  M. Koornneef,et al.  Sequential steps for developmental arrest in Arabidopsis seeds. , 2001, Development.

[132]  Da-Peng Zhang,et al.  The Mg-chelatase H subunit is an abscisic acid receptor , 2006, Nature.

[133]  Jan KeÇpczyński,et al.  Ethylene in seed dormancy and germination , 1997 .

[134]  M. Holdsworth,et al.  Post-genomics dissection of seed dormancy and germination. , 2008, Trends in plant science.

[135]  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.

[136]  M. Koornneef,et al.  Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh. , 1980, Theoretical and Applied Genetics.

[137]  Maarten Koornneef,et al.  The Absence of Histone H2B Monoubiquitination in the Arabidopsis hub1 (rdo4) Mutant Reveals a Role for Chromatin Remodeling in Seed Dormancy[W][OA] , 2007, The Plant Cell Online.

[138]  O. Van Wuytswinkel,et al.  Combined networks regulating seed maturation. , 2007, Trends in plant science.

[139]  Ayuko Kuwahara,et al.  Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. , 2006, The Plant journal : for cell and molecular biology.

[140]  C. M. Karssen,et al.  Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants , 1992, Plant Growth Regulation.

[141]  H. Truong,et al.  Nitrate, a signal relieving seed dormancy in Arabidopsis. , 2005, Plant, cell & environment.

[142]  C. M. Karssen,et al.  Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. , 1983, Planta.

[143]  M. Koornneef Giberillin-sensitive mutants in Arabidopsis thaliana , 1978 .

[144]  K. Shinozaki,et al.  ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. , 2007, The Plant journal : for cell and molecular biology.

[145]  Po-Pu Liu,et al.  Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. , 2005, The Plant journal : for cell and molecular biology.

[146]  M. Holdsworth,et al.  Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP , 2002, The EMBO journal.

[147]  K. Halliday,et al.  Cold and Light Control Seed Germination through the bHLH Transcription Factor SPATULA , 2005, Current Biology.

[148]  F. Chen,et al.  Expression of an expansin is associated with endosperm weakening during tomato seed germination. , 2000, Plant physiology.

[149]  Ayuko Kuwahara,et al.  Gibberellin Biosynthesis and Response during Arabidopsis Seed Germination Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011650. , 2003, The Plant Cell Online.

[150]  R. Huntley,et al.  D-type cyclins activate division in the root apex to promote seed germination in Arabidopsis , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[151]  P. McCourt,et al.  A role for brassinosteroids in germination in Arabidopsis. , 2001, Plant physiology.

[152]  L. Nehlin,et al.  Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box. , 2000, The Plant journal : for cell and molecular biology.

[153]  K. Onai,et al.  The lba1 mutation of UPF1 RNA helicase involved in nonsense-mediated mRNA decay causes pleiotropic phenotypic changes and altered sugar signalling in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[154]  Alisdair R. Fernie,et al.  Arabidopsis Seed Development and Germination Is Associated with Temporally Distinct Metabolic Switches1[W] , 2006, Plant Physiology.

[155]  E. Babiychuk,et al.  The Pleiotropic Role of the 26S Proteasome Subunit RPN10 in Arabidopsis Growth and Development Supports a Substrate-Specific Function in Abscisic Acid Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009217. , 2003, The Plant Cell Online.

[156]  Stefanie Tintelnot,et al.  Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. , 2006, Plant & cell physiology.

[157]  R. Gallagher,et al.  Dormancy release in Lolium rigidum seeds is a function of thermal after-ripening time and seed water content. , 2003, Functional plant biology : FPB.

[158]  U. Wobus,et al.  Molecular physiology of legume seed development. , 2005, Annual review of plant biology.

[159]  Jinrong Peng,et al.  Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis , 2005, Planta.

[160]  T. Hattori,et al.  A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[161]  P. Toorop,et al.  Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. , 2007, The Plant journal : for cell and molecular biology.

[162]  S. Meyer,et al.  A hydrothermal after-ripening time model for seed dormancy loss in Bromus tectorum L. , 2006, Seed Science Research.

[163]  T. Sun,et al.  Phytochrome Regulation and Differential Expression of Gibberellin 3β-Hydroxylase Genes in Germinating Arabidopsis Seeds , 1998, Plant Cell.

[164]  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.

[165]  Steven Penfield,et al.  Arabidopsis ABA INSENSITIVE4 Regulates Lipid Mobilization in the Embryo and Reveals Repression of Seed Germination by the Endosperm[W] , 2006, The Plant Cell Online.

[166]  Hans-Peter Mock,et al.  Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA , 2004, Planta.

[167]  M. West,et al.  Embryogenesis in Higher Plants: An Overview. , 1993, The Plant cell.

[168]  fusca3: A Heterochronic Mutation Affecting Late Embryo Development in Arabidopsis. , 1994, The Plant cell.

[169]  S. Kim,et al.  ABFs, a Family of ABA-responsive Element Binding Factors* , 2000, The Journal of Biological Chemistry.

[170]  A. Peeters,et al.  Characterization of mutants with reduced seed dormancy at two novel rdo loci and a further characterization of rdo1 and rdo2 in Arabidopsis. , 2002, Physiologia plantarum.

[171]  M. Ferrand,et al.  Stored mRNA in early embryos of a fern Marsilea vestita: A paternal and maternal origin , 1991, Molecular reproduction and development.

[172]  Alan M. Jones,et al.  G-Protein Complex Mutants Are Hypersensitive to Abscisic Acid Regulation of Germination and Postgermination Development1[W] , 2006, Plant Physiology.

[173]  S. Merlot,et al.  The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. , 1997, The Plant cell.

[174]  A. Yamamoto,et al.  LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. , 2005, Plant & cell physiology.

[175]  I. Ezcurra,et al.  Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression , 1999, Plant Molecular Biology.

[176]  K. Shinozaki,et al.  An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[177]  Wei Li,et al.  Response to Comment on "A G Protein–Coupled Receptor Is a Plasma Membrane Receptor for the Plant Hormone Abscisic Acid" , 2007, Science.

[178]  G. Leubner‐Metzger Functions and regulation of β-1,3-glucanases during seed germination, dormancy release and after-ripening , 2003, Seed Science Research.

[179]  D. Meinke,et al.  Leafy Cotyledon Mutants of Arabidopsis. , 1994, The Plant cell.

[180]  F. Meins,et al.  Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I β-1,3-glucanase during tobacco seed germination , 1998, Plant Molecular Biology.

[181]  M. Koornneef,et al.  Seed dormancy and germination. , 2002, Current opinion in plant biology.

[182]  S. Jacobsen,et al.  Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. , 1996, The Plant journal : for cell and molecular biology.

[183]  M. Holdsworth,et al.  Analysis of the role of COMATOSE and peroxisomal beta-oxidation in the determination of germination potential in Arabidopsis. , 2006, Journal of experimental botany.

[184]  T. Sun,et al.  Molecular mechanism of gibberellin signaling in plants. , 2004, Annual review of plant biology.

[185]  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.

[186]  Wei Wu,et al.  Gibberellin Mobilizes Distinct DELLA-Dependent Transcriptomes to Regulate Seed Germination and Floral Development in Arabidopsis1[W] , 2006, Plant Physiology.

[187]  M. Koornneef,et al.  Seed Dormancy and Germination , 2008, The arabidopsis book.

[188]  J. Ecker,et al.  DELLA Proteins and Gibberellin-Regulated Seed Germination and Floral Development in Arabidopsis1[w] , 2004, Plant Physiology.

[189]  S. Mansfield,et al.  The Dynamics of Seedling and Cotyledon Cell Development in Arabidopsis thaliana During Reserve Mobilization , 1996, International Journal of Plant Sciences.

[190]  J. Bewley Breaking down the walls — a role for endo-β-mannanase in release from seed dormancy? , 1997 .

[191]  THE EVOLUTIONARY ECOLOGY OF SEED GERMINATION OF ARABIDOPSIS THALIANA: VARIABLE NATURAL SELECTION ON GERMINATION TIMING , 2005, Evolution; international journal of organic evolution.

[192]  H. Kawaide,et al.  Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. , 1998, Plant physiology.

[193]  T. Sun,et al.  The Arabidopsis SLEEPY1 Gene Encodes a Putative F-Box Subunit of an SCF E3 Ubiquitin Ligase Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010827. , 2003, The Plant Cell Online.

[194]  H. Rolletschek,et al.  Dissection of a complex seed phenotype: novel insights of FUSCA3 regulated developmental processes. , 2008, Developmental biology.

[195]  J. Leymarie,et al.  Journal of Experimental Botany Advance Access published December 14, 2006 Journal of Experimental Botany, Page 1 of 13 , 2022 .

[196]  K. Bradford,et al.  Expression of a polygalacturonase associated with tomato seed germination. , 1999, Plant physiology.

[197]  Thomas Kroj,et al.  Regulation of storage protein gene expression in Arabidopsis , 2003, Development.

[198]  Colleen M Butler,et al.  A new role for phytochromes in temperature-dependent germination. , 2007, The New phytologist.

[199]  M. Hooks,et al.  The Arabidopsis ALDP protein homologue COMATOSE is instrumental in peroxisomal acetate metabolism. , 2007, The Biochemical journal.