Plant hormone interactions during seed dormancy release and germination

This review focuses mainly on eudicot seeds, and on the interactions between abscisic acid (ABA), gibberellins (GA), ethylene, brassinosteroids (BR), auxin and cytokinins in regulating the interconnected molecular processes that control dormancy release and germination. Signal transduction pathways, mediated by environmental and hormonal signals, regulate gene expression in seeds. Seed dormancy release and germination of species with coat dormancy is determined by the balance of forces between the growth potential of the embryo and the constraint exerted by the covering layers, e.g. testa and endosperm. Recent progress in the field of seed biology has been greatly aided by molecular approaches utilizing mutant and transgenic seeds of Arabidopsis thaliana and the Solanaceae model systems, tomato and tobacco, which are altered in hormone biology. ABA is a positive regulator of dormancy induction and most likely also maintenance, while it is a negative regulator of germination. GA releases dormancy, promotes germination and counteracts ABA effects. Ethylene and BR promote seed germination and also counteract ABA effects. We present an integrated view of the molecular genetics, physiology and biochemistry used to unravel how hormones control seed dormancy release and germination.

[1]  S. Rood,et al.  Plant Growth Substances 1988 , 1990, Springer Berlin Heidelberg.

[2]  M. Ohta,et al.  Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. , 2000, The Plant journal : for cell and molecular biology.

[3]  P. Toorop,et al.  The second step of the biphasic endosperm cap weakening that mediates tomato (Lycopersicon esculentum) seed germination is under control of ABA. , 2000, Journal of experimental botany.

[4]  C. M. Karssen,et al.  Gibberellins regulate seed germination in tomato by endosperm weakening: a study with gibberellin-deficient mutants , 1987, Planta.

[5]  K. Bradford,et al.  Class I beta-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. , 2001, Plant physiology.

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

[7]  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.

[8]  H J Klee,et al.  Differential regulation of the tomato ETR gene family throughout plant development. , 1998, The Plant journal : for cell and molecular biology.

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

[10]  J. Alonso,et al.  Ethylene signalling and response pathway: a unique signalling cascade with a multitude of inputs and outputs , 2005 .

[11]  I. Yamaguchi,et al.  Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds , 1993, Journal of Plant Growth Regulation.

[12]  S. Gan,et al.  A novel zinc-finger protein with a proline-rich domain mediates ABA-regulated seed dormancy in Arabidopsis , 2004, Plant Molecular Biology.

[13]  C. M. Karssen,et al.  The role of endogenous gibberellin in seed and fruit development of tomato: Studies with a gibberellin‐deficient mutant , 1987 .

[14]  M. E. Foley,et al.  Genetic and physiological evidence for the role of gibberellic acid in the germination of dormant Avena fatua seeds. , 1998 .

[15]  N. Olszewski,et al.  Two O-linked N-acetylglucosamine transferase genes of Arabidopsis thaliana L. Heynh. have overlapping functions necessary for gamete and seed development. , 2002, Genetics.

[16]  E. García-Olivares,et al.  1-aminocyclopropane-1-carboxylate oxidase from embryonic axes of germinating chick-pea (Cicer arietinum L.) seeds: cellular immunolocalization and alterations in its expression by indole-3-acetic acid, abscisic acid and spermine , 2001, Seed Science Research.

[17]  J.R.N. Taylor,et al.  Changes in selected plant growth regulators during germination in sorghum , 1998, Seed Science Research.

[18]  T. Endo,et al.  Restoration of Seed Germination at Supraoptimal Temperatures by Fluridone, an Inhibitor of Abscisic Acid Biosynthesis , 1998 .

[19]  A. Marion-Poll,et al.  Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia , 2004, Planta.

[20]  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.

[21]  M. C. Giallorenzi,et al.  Termination of hull-imposed dormancy in developing barley grains is correlated with changes in embryonic ABA levels and sensitivity , 1999, Seed Science Research.

[22]  M. Szekeres.  Brassinosteroid and systemin: two hormones perceived by the same receptor. , 2003, Trends in plant science.

[23]  C. Kunz,et al.  Distinct ethylene- and tissue-specific regulation of β-1,3-glucanases and chitinases during pea seed germination , 1999, Planta.

[24]  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.

[25]  D. Hays,et al.  The role of gibberellins in embryo axis development. , 2002, Journal of experimental botany.

[26]  H. Goodman,et al.  The Arabidopsis Abscisic Acid Response Locus ABI4 Encodes an APETALA2 Domain Protein , 1998, Plant Cell.

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

[28]  Caren Chang,et al.  Arabidopsis RGL1 Encodes a Negative Regulator of Gibberellin Responses Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010325. , 2002, The Plant Cell Online.

[29]  Klaus Harter,et al.  Plant Two-Component Signaling Systems and the Role of Response Regulators1 , 2002, Plant Physiology.

[30]  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.

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

[32]  I. Baldwin,et al.  Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata , 2004, Seed Science Research.

[33]  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.

[34]  K. Bradford,et al.  A germination-specific endo-beta-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. , 2000, Plant physiology.

[35]  J. Giraudat,et al.  ABSCISIC ACID SIGNAL TRANSDUCTION. , 1998, Annual review of plant physiology and plant molecular biology.

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

[37]  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.

[38]  E. Schäfer,et al.  Spatial and temporal pattern of light‐regulated gene expression during tobacco seedling development: the photosystem II‐related genes Lhcb (Cab) and PsbP (Oee2) , 1995 .

[39]  T. Lynch,et al.  Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. , 2000, Plant physiology.

[40]  J. B. Reid,et al.  Gibberellins are required for embryo growth and seed development in pea , 1997 .

[41]  C. Rivin,et al.  Gibberellins and seed development in maize. II. Gibberellin synthesis inhibition enhances abscisic acid signaling in cultured embryos. , 2000, Plant physiology.

[42]  M. Jullien,et al.  Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance , 2000, Planta.

[43]  R. Geneve,et al.  Seed germination of ethylene perception mutants of tomato and Arabidopsis , 2003, Seed Science Research.

[44]  G. Leubner-Metzger,et al.  Brassinosteroids Promote Seed Germination , 2003 .

[45]  A. Thompson,et al.  Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. , 2000, The Plant journal : for cell and molecular biology.

[46]  C. M. Karssen,et al.  The Benefit of Biosynthesis and Response Mutants to the Study of the Role of Abscisic Acid in Plants , 1990 .

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

[48]  R. E. Sharp,et al.  Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. , 2000, Plant physiology.

[49]  D. Nevins,et al.  Endo-[beta]-Mannanase Activity Present in Cell Wall Extracts of Lettuce Endosperm prior to Radicle Emergence , 1997, Plant physiology.

[50]  C. Camilleri,et al.  Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. , 2000, Genes & development.

[51]  J. M. Nelson,et al.  Stimulation of tomato, pepper and sugarbeet seed germination at low temperatures by growth regulators. , 1980 .

[52]  F. Harren,et al.  On the Role of Ethylene in Seed Germination and Early RootGrowth of Pisum sativum , 1995 .

[53]  M. Koornneef,et al.  Arabidopsis Mutants with a Reduced Seed Dormancy , 1996, Plant physiology.

[54]  U. Conrad,et al.  Seed‐specific immunomodulation of abscisic acid activity induces a developmental switch , 1997, The EMBO journal.

[55]  T. Altmann.  Molecular physiology of brassinosteroids revealed by the analysis of mutants , 1999, Planta.

[56]  Jinrong Peng,et al.  The role of GA-mediated signalling in the control of seed germination. , 2002, Current opinion in plant biology.

[57]  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.

[58]  M. Serek,et al.  Compounds Interacting with the Ethylene Receptor in Plants , 2003 .

[59]  T. Yokota,et al.  Brassinosteroids. Chemistry, bioactivity, and applications. , 1991 .

[60]  Yi-feng Chen,et al.  Ethylene signal transduction. , 2005, Annals of botany.

[61]  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.

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

[63]  H. Hirt,et al.  A MAPK pathway mediates ethylene signaling in plants , 2003, The EMBO journal.

[64]  M. Cohn,et al.  Seed Dormancy in Red Rice (Oryza sativa). II. Response to Cytokinins , 1982, Weed Science.

[65]  C. M. Karssen,et al.  A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. , 1986 .

[66]  K. Yamaguchi-Shinozaki,et al.  Analysis of an ABA-responsive rice gene promoter in transgenic tobacco , 1990, Plant Molecular Biology.

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

[68]  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.

[69]  A. Matilla,et al.  The heterogeneity of turnip-tops (Brassica rapa) seeds inside the silique affects germination, the activity of the final step of the ethylene pathway, and abscisic acid and polyamine content. , 2003, Functional plant biology : FPB.

[70]  K. Palme,et al.  Auxin and the developing root of Arabidopsis thaliana , 2005 .

[71]  A. Marion-Poll,et al.  Molecular biology and regulation of abscisic acid biosynthesis in plants , 1999 .

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

[73]  G. Leubner-Metzger,et al.  Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways , 2001, Planta.

[74]  E. Cervantes,et al.  Ethylene regulates the expression of a cysteine proteinase gene during germination of chickpea (Cicer arietinum L.) , 1994, Plant Molecular Biology.

[75]  Caren Chang.  Ethylene signaling: the MAPK module has finally landed. , 2003, Trends in plant science.

[76]  K. Yoneyama,et al.  Fluridone and norflurazon, carotenoid-biosynthesis inhibitors, promote seed conditioning and germination of the holoparasite Orobanche minor. , 2004, Physiologia plantarum.

[77]  A. Matilla.  Ethylene in seed formation and germination , 2000, Seed Science Research.

[78]  K. Ljung,et al.  Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. , 2001, Plant physiology.

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

[80]  M. Montagu,et al.  The ABSCISIC ACID‐INSENSITIVE 3 (ABI3) gene is expressed during vegetative quiescence processes in Arabidopsis , 1999 .

[81]  C. M. Karssen,et al.  Effects of light and temperature on seed dormancy and gibberellin‐stimulated germination in Arabidopsis thaliana: studies with gibberellin‐deficient and ‐insensitive mutants. , 1993 .

[82]  N. Fedoroff,et al.  Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[83]  M. Estelle,et al.  Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana , 1988, Science.

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

[85]  C. M. Karssen,et al.  Key Role for Endogenous Gibberellins in the Control of Seed Germination , 1989 .

[86]  S. Naito,et al.  Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. , 1998, Plant & cell physiology.

[87]  H. Saini,et al.  Control processes in the induction and relief of thermoinhibition of lettuce seed germination : actions of phytochrome and endogenous ethylene. , 1989, Plant physiology.

[88]  A. Marion-Poll,et al.  Engineering seed dormancy by the modification of zeaxanthin epoxidase gene expression , 1999, Plant Molecular Biology.

[89]  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.

[90]  L. Kaufman,et al.  The Arabidopsis cupin domain protein AtPirin1 interacts with the G protein alpha-subunit GPA1 and regulates seed germination and early seedling development. , 2003, The Plant cell.

[91]  J. Ross,et al.  New interactions between classical plant hormones. , 2001, Trends in plant science.

[92]  F. Meins,et al.  Sense transformation reveals a novel role for class I beta-1, 3-glucanase in tobacco seed germination. , 2000, The Plant journal : for cell and molecular biology.

[93]  Nam-Hai Chua,et al.  The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. , 2005, Genes & development.

[94]  R. Finkelstein.  Maternal Effects Govern Variable Dominance of Two Abscisic Acid Response Mutations in Arabidopsis thaliana , 1994, Plant physiology.

[95]  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.

[96]  T. Altmann,et al.  Brassinosteroids from seeds of Arabidopsis thaliana. , 1997, Phytochemistry.

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

[98]  H. Kawaide,et al.  Abscisic acid in the thermoinhibition of lettuce seed germination and enhancement of its catabolism by gibberellin. , 2003, Journal of experimental botany.

[99]  T. Sun,et al.  Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. , 2001, Genetics.

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

[101]  J. B. Reid,et al.  Abscisic acid levels in seeds of the gibberellin-deficient mutant lh-2 of pea (Pisum sativum) , 1999 .

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

[103]  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.

[104]  Kjell Stålberg,et al.  Seed-Specific Overexpression of an Endogenous Arabidopsis Phytoene Synthase Gene Results in Delayed Germination and Increased Levels of Carotenoids, Chlorophyll, and Abscisic Acid1 , 2003, Plant Physiology.

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

[106]  M. Cohn.  Operational and philosophical decisions in seed dormancy research , 1996, Seed Science Research.

[107]  P. Schopfer,et al.  Effect of Water Stress, Seed Coat Restraint, and Abscisic Acid upon Different Germination Capabilities of Two Tomato Lines at Low Temperature. , 1983, Plant physiology.

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

[109]  A. Kermode,et al.  Role of an ABI3 homologue in dormancy maintenance of yellow-cedar seeds and in the activation of storage protein and Em gene promoters , 2004, Plant Molecular Biology.

[110]  Masaharu Suzuki,et al.  Viviparous1 Alters Global Gene Expression Patterns through Regulation of Abscisic Acid Signaling1[w] , 2003, Plant Physiology.

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

[112]  S. Jones-Held,et al.  Brassinolide application to Lepidium sativum seeds and the effects on seedling growth , 1996, Journal of Plant Growth Regulation.

[113]  A. Itai,et al.  Germination strategy of Striga hermonthica involves regulation of ethylene biosynthesis , 2003 .

[114]  J. Slovin,et al.  A gene encoding a protein modified by the phytohormone indoleacetic acid , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[117]  T. Lynch,et al.  Regulatory Networks in Seeds Integrating Developmental, Abscisic Acid, Sugar, and Light Signaling1 , 2003, Plant Physiology.

[118]  T. Lynch,et al.  The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 Locus Encodes a Novel Protein Mediating Abscisic Acid and Sugar Responses Essential for Growth On-line version contains Web-only data. , 2004, The Plant Cell Online.

[119]  C. Kao,et al.  Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. , 2002, The Plant journal : for cell and molecular biology.

[120]  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.

[121]  G. Leubner-Metzger,et al.  Seed after-ripening and over-expression of class I β-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release , 2002, Planta.

[122]  P. Hedden,et al.  Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. , 2000, Plant physiology.

[123]  T. Sun,et al.  The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. , 1997, Genetics.

[124]  S. Abrams,et al.  Changes in ABA turnover and sensitivity that accompany dormancy termination of yellow-cedar (Chamaecyparis nootkatensis) seeds. , 2002, Journal of experimental botany.

[125]  A. Rohde,et al.  ABI3 emerges from the seed. , 2000, Trends in plant science.

[126]  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.

[127]  L. Strader,et al.  Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[128]  L. Young,et al.  Characterization and expression of plasma and tonoplast membrane aquaporins in primed seed of Brassica napus during germination under stress conditions , 1999, Plant Molecular Biology.

[129]  C. Preston,et al.  Methyl Jasmonate as an Allelopathic Agent: Sagebrush Inhibits Germination of a Neighboring Tobacco, Nicotiana Attenuata , 2002, Journal of Chemical Ecology.

[130]  G. M. Paulsen,et al.  Relationship of indoleacetic acid and tryptophan to dormancy and preharvest sprouting of wheat. , 2003, Functional plant biology : FPB.

[131]  J. Schroeder,et al.  Localization, Ion Channel Regulation, and Genetic Interactions during Abscisic Acid Signaling of the Nuclear mRNA Cap-Binding Protein, ABH11 , 2002, Plant Physiology.

[132]  M. Koornneef,et al.  Characterization of green seed, an Enhancer of abi3-1 in Arabidopsis That Affects Seed Longevity1 , 2003, Plant Physiology.

[133]  M. Talón,et al.  Gibberellin-ethylene interaction controls radial expansion in citrus roots , 1997, Planta.

[134]  Y. Kamiya,et al.  Gibberellins and Light-Stimulated Seed Germination , 2001, Journal of Plant Growth Regulation.

[135]  D. Berner,et al.  In Vitro Germination of Striga hermonthica and Striga aspera Seeds by 1-Aminocyclopropane-1-Carboxylic Acid , 2003, Natural product research.

[136]  J. Cohen,et al.  Auxin Biosynthesis during Seed Germination in Phaseolus vulgaris. , 1992, Plant physiology.

[137]  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.

[138]  L. Baumbusch,et al.  LEC1, FUS3, ABI3 and Em expression reveals no correlation with dormancy in Arabidopsis. , 2003, Journal of experimental botany.

[139]  Peter McCourt,et al.  The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

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

[141]  Y. Esashi,et al.  Ethylene Production in Pea and Cocklebur Seeds of Differing Vigour , 1991 .

[142]  P. Hugueney,et al.  Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. , 1996, The EMBO journal.

[143]  H. Hilhorst.  A critical update on seed dormancy. I. Primary dormancy , 1995, Seed Science Research.

[144]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings , 2002 .

[145]  M. Mok,et al.  CYTOKININ METABOLISM AND ACTION. , 2003, Annual review of plant physiology and plant molecular biology.

[146]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[147]  J. Ecker,et al.  Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. , 1998, Genes & development.

[148]  H. Kawaide,et al.  Deactivation of Gibberellin by 2-Oxidation during Germination of Photoblastic Lettuce Seeds , 2003, Bioscience, biotechnology, and biochemistry.

[149]  Carlos Nicolás,et al.  Molecular cloning of a functional protein phosphatase 2C (FsPP2C2) with unusual features and synergistically up-regulated by ABA and calcium in dormant seeds of Fagus sylvatica. , 2002, Physiologia plantarum.

[150]  I. Romagosa,et al.  Dormancy, ABA content and sensitivity of a barley mutant to ABA application during seed development and after ripening. , 2001, Journal of experimental botany.

[151]  H. Hilhorst,et al.  Primary dormancy in tomato (Lycopersicon esculentum cv. Moneymaker): studies with the sitiens mutant , 1996 .

[152]  J. Bewley,et al.  The relationship between beta-mannosidase and endo-beta-mannanase activities in tomato seeds during and following germination: a comparison of seed populations and individual seeds. , 2003, Journal of experimental botany.

[153]  P. McCourt,et al.  Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. , 1998, Genetics.

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

[155]  Miguel González-Guzmán,et al.  Two New Alleles of the abscisic aldehyde oxidase 3 Gene Reveal Its Role in Abscisic Acid Biosynthesis in Seeds1 , 2004, Plant Physiology.

[156]  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.

[157]  A. D. Worsham,et al.  Effects of Brassinolide on Conditioning and Germination of Witchweed (Striga asiatica) Seeds , 1991 .

[158]  S. Bhojwani,et al.  Current Trends in the Embryology of Angiosperms , 2001, Springer Netherlands.

[159]  B. Hess,et al.  A role for reactive oxygen species in endosperm weakening. , 2007 .

[160]  R. Benech-Arnold,et al.  Hormonal Regulation of Dormancy in Developing Sorghum Seeds , 1997, Plant physiology.

[161]  M. E. Foley,et al.  Genetic and molecular control of seed dormancy , 1997 .

[162]  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.

[163]  H. Nonogaki,et al.  Endo-β-mannanase activity is associated with the completion of embryogenesis in imbibed carrot (Daucus carota L.) seeds , 2003, Seed Science Research.

[164]  Yongqing Ma,et al.  Conditioning period, CO2 and GR24 influence ethylene biosynthesis and germination of Striga hermonthica , 2000 .

[165]  D. McCarty.  Genetic control and integration of maturation and germination pathways in seed development , 1995 .

[166]  Nam-Hai Chua,et al.  IMB1, a bromodomain protein induced during seed imbibition, regulates ABA- and phyA-mediated responses of germination in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[167]  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.

[168]  J. G. Scandalios,et al.  Catalase gene expression in response to auxin-mediated developmental signals. , 2002, Physiologia plantarum.

[169]  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.

[170]  C. Schwechheimer,et al.  The regulation of transcription factor activity in plants , 1998 .

[171]  M. Hall.  Ethylene and seed germination , 1975 .

[172]  A. D. Worsham,et al.  Effects of brassinosteroids on conditioning and germination of clover broomrape (Orobanche minor) seeds , 1995, Plant Growth Regulation.

[173]  P. McCourt,et al.  A Protein Farnesyl Transferase Involved in Abscisic Acid Signal Transduction in Arabidopsis , 1996, Science.

[174]  L. J. Audus.  Plant growth substances , 1954 .

[175]  A. Basra.  Handbook of Seed Science and Technology , 2007 .

[176]  I. Graham,et al.  Germination and storage reserve mobilization are regulated independently in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[177]  T. Altmann,et al.  Brassinosteroids Promote Root Growth in Arabidopsis , 2003, Plant Physiology.

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

[179]  J. Bewley,et al.  A distinction between the actions of abscisic acid, gibberellic acid and cytokinins in light-sensitive lettuce seed , 1972, Planta.

[180]  P. McCourt,et al.  A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana. , 2002, Genetics.

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

[182]  T. Sun,et al.  The Arabidopsis SLEEPY 1 Gene Encodes a Putative F-Box Subunit of an SCF E 3 Ubiquitin Ligase , 2003 .

[183]  K. Bradford,et al.  Germination and Dormancy of Abscisic Acid- and Gibberellin-Deficient Mutant Tomato (Lycopersicon esculentum) Seeds (Sensitivity of Germination to Abscisic Acid, Gibberellin, and Water Potential) , 1993, Plant physiology.

[184]  S. Abrams,et al.  Vicilin and Napin Storage-Protein Gene Promoters Are Responsive to Abscisic Acid in Developing Transgenic Tobacco Seed but Lose Sensitivity following Premature Desiccation , 1996, Plant physiology.

[185]  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.

[186]  M. Holdsworth,et al.  Genetic control mechanisms regulating the initiation of germination , 2001 .

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

[188]  R. Ranjan,et al.  Jasmonic acid affects dormancy and sugar catabolism in germinating apple embryos , 2002 .

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

[190]  J. Vandekerckhove,et al.  Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. , 2002, Physiologia plantarum.

[191]  Guillaume Lambert,et al.  The Homologous ABI5 and EEL Transcription Factors Function Antagonistically to Fine-Tune Gene Expression during Late Embryogenesis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000869. , 2002, The Plant Cell Online.

[192]  M. Holdsworth,et al.  Identification and analysis of proteins that interact with the Avena fatua homologue of the maize transcription factor VIVIPAROUS 1. , 2000, The Plant journal : for cell and molecular biology.

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

[194]  T. Sun,et al.  The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. , 1994, The Plant cell.

[195]  T. Housley,et al.  Striga asiatica seed conditioning and 1‐aminocyclopropane‐1‐carboxylate oxidase activity , 2001 .

[196]  J. Chory,et al.  Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1 , 2005, Nature.

[197]  S. Swain,et al.  Altered expression of SPINDLY affects gibberellin response and plant development. , 2001, Plant physiology.

[198]  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.

[199]  R. Emery,et al.  The forms and sources of cytokinins in developing white lupine seeds and fruits. , 2000, Plant physiology.

[200]  T. Ait-Ali,et al.  HOW GIBBERELLIN REGULATES PLANT GROWTH AND DEVELOPMENT: A Molecular Genetic Analysis of Gibberellin Signaling. , 2001, Annual review of plant physiology and plant molecular biology.

[201]  M. Caboche,et al.  Characterization of three hormone mutants of Nicotiana plumbaginifolia: evidence for a common ABA deficiency , 1992, Theoretical and Applied Genetics.

[202]  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.

[203]  I. Coraggio,et al.  Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase , 2000, Planta.

[204]  M. Bopp.  Plant Growth Substances 1985 , 1986, Proceedings in Life Sciences.

[205]  H. Klee,et al.  Ethylene Signal Transduction. Moving beyond Arabidopsis , 2004, Plant Physiology.

[206]  L. Mur,et al.  Ethylene signal perception and transduction: multiple paradigms? , 2001, Biological reviews of the Cambridge Philosophical Society.

[207]  A. Basra,et al.  Hormonal interactions during seed dormancy release and germination. , 2006 .

[208]  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.

[209]  J. Derek Bewleyl,et al.  Seed Germination and Dormancy , 2002 .

[210]  J. Bewley,et al.  Exogenous gibberellins inhibit coffee (Coffea arabica cv. Rubi) seed germination and cause cell death in the embryo. , 2005, Journal of experimental botany.

[211]  S. J. Ambrose,et al.  Dormancy termination of western white pine (Pinus monticola Dougl. Ex D. Don) seeds is associated with changes in abscisic acid metabolism , 2004, Planta.

[212]  T. Hall,et al.  The 5′ UTR negatively regulates quantitative and spatial expression from the ABI3 promoter , 2004, Plant Molecular Biology.

[213]  P. McCourt,et al.  A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele , 1992 .

[214]  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.

[215]  S. Yamaguchi,et al.  Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. , 2002, The Plant journal : for cell and molecular biology.

[216]  A. Izhaki,et al.  The role of SPY and its TPR domain in the regulation of gibberellin action throughout the life cycle of Petunia hybrida plants. , 2001, The Plant journal : for cell and molecular biology.

[217]  P. Schopfer,et al.  Control of Seed Germination by Abscisic Acid : II. Effect on Embryo Water Uptake in Brassica napus L. , 1984, Plant physiology.

[218]  L. Petruzzelli,et al.  Calcium requirement for ethylene-dependent responses involving 1-aminocyclopropane-1-carboxylic acid oxidase in radicle tissues of germinated pea seeds , 2003 .

[219]  Heribert Hirt,et al.  Plant PP2C phosphatases: emerging functions in stress signaling. , 2004, Trends in plant science.

[220]  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.

[221]  C. Nicolás,et al.  Evidence of a cross-talk regulation of a GA 20-oxidase (FsGA20ox1) by gibberellins and ethylene during the breaking of dormancy in Fagus sylvatica seeds. , 2004, Physiologia plantarum.

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

[223]  I. Baldwin,et al.  Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual, Nicotiana attenuata , 2002, Seed Science Research.

[224]  P. Weisbeek,et al.  The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. , 2000, The Plant journal : for cell and molecular biology.

[225]  S. Gibson,et al.  ABA and sugar interactions regulating development: cross-talk or voices in a crowd? , 2002, Current opinion in plant biology.

[226]  L. Petruzzelli,et al.  Distinct expression patterns of β-1,3-glucanases and chitinases during the germination of Solanaceous seeds , 2003, Seed Science Research.

[227]  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.

[228]  P. Toorop,et al.  Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination , 2004, Planta.

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

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

[231]  G. Engler,et al.  Differentially expressed genes associated with dormancy or germination of Arabidopsis thaliana seeds , 2005, Planta.

[232]  Y. Kamiya,et al.  Regulation of gibberellin biosynthesis by light. , 1999, Current opinion in plant biology.

[233]  F. Parcy,et al.  Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation. , 2005, Journal of experimental botany.