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Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination

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Abstract

Appropriate responses of seeds and fruits to environmental factors are key traits that control the establishment of a species in a particular ecosystem. Adaptation of germination to abiotic stresses and changing environmental conditions is decisive for fitness and survival of a species. Two opposing forces provide the basic physiological mechanism for the control of seed germination: the increasing growth potential of the embryo and the restraint weakening of the various covering layers (seed envelopes), including the endosperm which is present to a various extent in the mature seeds of most angiosperms. Gibberellins (GA), abscisic acid (ABA) and ethylene signaling and metabolism mediate environmental cues and in turn influence developmental processes like seed germination. Cross-species work has demonstrated that GA, ABA and ethylene interact during the regulation of endosperm weakening, which is at least partly based on evolutionarily conserved mechanisms. We summarize the recent progress made in unraveling how ethylene promotes germination and acts as an antagonist of ABA. Far less is known about jasmonates in seeds for which we summarize the current knowledge about their role in seeds. While it seems very clear that jasmonates inhibit germination, the results obtained so far are partly contradictory and depend on future research to reach final conclusions on the mode of jasmonate action during seed germination. Understanding the mechanisms underlying the control of seed germination and its hormonal regulation is not only of academic interest, but is also the ultimate basis for further improving crop establishment and yield, and is therefore of common importance.

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References

  • Adams E, Turner J (2010) COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp Bot 61(15):4373–4386

    Article  PubMed  CAS  Google Scholar 

  • Adham AR, Zolman BK, Millius A, Bartel B (2005) Mutations in Arabidopsis acyl-CoA oxidase genes reveal distinct and overlapping roles in β-oxidation. Plant J 41(6):859–874

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Ecker JR (2001) The ethylene pathway: a paradigm for plant hormone signaling and interaction. Science’s STKE 2001 (70):RE1

  • Argyris J, Dahal P, Hayashi E, Still DW, Bradford KJ (2008) Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiol 148(2):926–947

    Article  PubMed  CAS  Google Scholar 

  • Argyris J, Truco M, Ochoa O, McHale L, Dahal P, Van Deynze A, Michelmore R, Bradford K (2011) A gene encoding an abscisic acid biosynthetic enzyme LsNCED4 collocates with the high temperature germination locus Htg6.1 in lettuce (Lactuca sp.). TAG Theor Appl Genet 122(1):95–108

    Article  CAS  Google Scholar 

  • Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14(02):93–107

    Article  CAS  Google Scholar 

  • Balbi V, Devoto A (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 177(2):301–318

    Article  PubMed  CAS  Google Scholar 

  • Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150(2):1006–1021

    Article  PubMed  CAS  Google Scholar 

  • Bassel GW, Mullen RT, Bewley JD (2006) ABI3 expression ceases following, but not during, germination of tomato and Arabidopsis seeds. J Exp Bot 57:1291–1297

    Article  PubMed  CAS  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12(7):1103–1116

    Article  PubMed  CAS  Google Scholar 

  • Berger S, Bell E, Mullet JE (1996) Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiol 111(2):525–531

    PubMed  CAS  Google Scholar 

  • Bethke PC, Libourel IGL, Aoyama N, Chung Y–Y, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143(3):1173–1188

    Article  PubMed  CAS  Google Scholar 

  • Bewley JD (1997a) Breaking down the walls—a role for endo-β-mannanase in release from seed dormancy? Trends Plant Sci 2(12):464–469

    Article  Google Scholar 

  • Bewley JD (1997b) Seed germination and dormancy. Plant Cell 9(7):1055–1066

    Article  PubMed  CAS  Google Scholar 

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60(1):183–205

    Article  PubMed  CAS  Google Scholar 

  • Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE (2006) Gene expression profiles of Arabidopsis Cvi seed during cycling through dormant and non-dormant states indicate a common underlying dormancy control mechanism. Plant J 46:805–822

    Article  PubMed  CAS  Google Scholar 

  • Calvo AP, Nicolás C, Nicolás G, Rodríguez D (2004) 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. Physiol Plant 120(4):623–630

    Article  PubMed  CAS  Google Scholar 

  • Cao D, Hussain A, Cheng H, Peng J (2005) Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis. Planta 223(1):105–113

    Article  PubMed  CAS  Google Scholar 

  • Carrera E, Holman T, Medhurst A, Peer W, Schmuths H, Footitt S, Theodoulou FL, Holdsworth MJ (2007) Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination. Plant Physiol 143(4):1669–1679

    Article  PubMed  CAS  Google Scholar 

  • Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 53:214–224

    Article  PubMed  CAS  Google Scholar 

  • Chao WS, Gu Y-Q, Pautot V, Bray EA, Walling LL (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120(4):979–992

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Bradford KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiol 124:1265–1274

    Article  PubMed  CAS  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448(7154):666–671

    Article  PubMed  CAS  Google Scholar 

  • Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) 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. Plant J 42(1):35–48

    Article  PubMed  CAS  Google Scholar 

  • Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146(3):952–964

    Article  PubMed  CAS  Google Scholar 

  • Crane PR, Friis EM, Pedersen KR (1995) The origin and early diversification of angiosperms. Nature 374(6517):27–33

    Article  CAS  Google Scholar 

  • da Silva EAA, Toorop PE, van Aelst AC, Hilhorst HWM (2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination. Planta 220(2):251–261

    Article  PubMed  CAS  Google Scholar 

  • da Silva EAA, Toorop PE, Van Lammeren AAM, Hilhorst HWM (2008) ABA inhibits embryo cell expansion and early cell division events during coffee (Coffea arabica ‘Rubi’) seed germination. Ann Bot 102(3):425–433

    Article  PubMed  CAS  Google Scholar 

  • Dave A, Hernandez ML, He Z, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23(2):583–599

    Article  PubMed  CAS  Google Scholar 

  • Debaene-Gill SB, Allen PS, Gardner JS (1994) Morphology of the perennial ryegrass (Lolium perenne; Poaceae) coleorhiza and emerging radicle with continuous or discontinuous hydration. Am J Bot 81(6):739–744

    Article  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122(2):403–414

    Article  PubMed  CAS  Google Scholar 

  • Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana—enzymes, products, regulation. Plant Biol 8(3):297–306

    Article  PubMed  CAS  Google Scholar 

  • Depuydt S, Hardtke S (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21(9):R365–R373

    Article  PubMed  CAS  Google Scholar 

  • Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin–ligase complex in Arabidopsis. Plant J 32(4):457–466

    Article  PubMed  CAS  Google Scholar 

  • Dutta S, Bradford KJ, Nevins DJ (1994) Cell-wall autohydrolysis in isolated endosperms of lettuce (Lactuca sativa L.). Plant Physiol 104(2):623–628

    PubMed  CAS  Google Scholar 

  • Ellis C, Turner J (2002) A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215(4):549–556

    Article  PubMed  CAS  Google Scholar 

  • Etheridge N, Hall B, Schaller G (2006) Progress report: ethylene signaling and responses. Planta 223(3):387–391

    Article  PubMed  CAS  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6(5):751–759

    Article  PubMed  CAS  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171(3):501–523

    Article  PubMed  CAS  Google Scholar 

  • Fonseca S, Chico JM, Solano R (2009a) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12(5):539–547

    Article  PubMed  CAS  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009b) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5(5):344–350

    Article  PubMed  CAS  Google Scholar 

  • Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J 21(12):2912–2922

    Article  PubMed  CAS  Google Scholar 

  • Forbis TA, Floyd SK, Queiroz Ad (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56(11):2112–2125

    PubMed  Google Scholar 

  • Friedman WE (1998) The evolution of double fertilization and endosperm: an ‘historical’ perspective. Sex Plant Reprod 11(1):6–16

    Article  Google Scholar 

  • Fry SC, Dumville JC, Miller JG (2001) Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. Biochem J 357(Pt 3):729–737

    Article  PubMed  CAS  Google Scholar 

  • Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J (2004) Peroxisomal acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell Online 16(2):394–405

    Article  CAS  Google Scholar 

  • Gallardo M, Gallardo ME, Matilla A, Munoz de Ruedo P, Sanchez-Calle IM (1994) Inhibition of polyamine synthesis by cyclohexylamine stimulates the ethylene pathway and accelerates the germination of Cicer arietinum seeds. Physiol Plant 91:9–16

    Article  CAS  Google Scholar 

  • Gallardo M, Sanchez-Calle IM, Munoz de Ruedo P, Matilla A (1996) Alleviation of thermoinhibition in chick-pea seeds by putrescine involves the ethylene pathway. Aust J Plant Physiol 23:479–487

    Article  CAS  Google Scholar 

  • Gerjets T, Scholefield D, Foulkes MJ, Lenton JR, Holdsworth MJ (2010) An analysis of dormancy, ABA responsiveness, after-ripening and pre-harvest sprouting in hexaploid wheat (Triticum aestivum L.) caryopses. J Exp Bot 61(2):597–607

    Article  PubMed  CAS  Google Scholar 

  • Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12(7):1117–1126

    Article  PubMed  CAS  Google Scholar 

  • Graeber K, Linkies A, Müller K, Wunchova A, Rott A, Leubner-Metzger G (2010) Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol 73(1):67–87

    Article  PubMed  CAS  Google Scholar 

  • Groot SPC, Karssen CM (1992) Dormancy and germination of abscisic acid-deficient tomato seeds. Plant Physiol 99:952–958

    Article  PubMed  CAS  Google Scholar 

  • Groot SPC, Bruinsma J, Karssen CM (1987) The role of endogenous gibberellin in seed and fruit development of tomato: studies with a gibberellin-deficient mutant. Physiol Plant 71(2):184–190

    Article  CAS  Google Scholar 

  • Hauser F, Waadt R, Schroeder Julian I (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21(9):R346–R355

    Article  PubMed  CAS  Google Scholar 

  • Hepher A, Roberts JA (1985a) The control of seed germination in Trollius ledebouri: a model of seed dormancy. Planta 166(3):321–328

    Article  CAS  Google Scholar 

  • Hepher A, Roberts JA (1985b) The control of seed germination in Trollius ledebouri: the breaking of dormancy. Planta 166(3):314–320

    Article  CAS  Google Scholar 

  • Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Hess B, Machackova I, Fischer U, Leubner-Metzger G (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot 58:3047–3060

    Article  PubMed  CAS  Google Scholar 

  • Hilhorst HWM, Downie B (1995) Primary dormancy in tomato (Lycopersicon esculentum cv. Moneymaker): studies with the sitiens mutant. J Exp Bot 47(294):89–97

    Google Scholar 

  • Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. Plant Cell 19(10):3058–3079. doi:10.1105/tpc.107.051524

    Article  PubMed  CAS  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJJ (2008a) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179(1):33–54

    Article  PubMed  CAS  Google Scholar 

  • Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008b) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13(1):7–13

    Article  PubMed  CAS  Google Scholar 

  • Iglesias-Fernández R, Matilla A (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellin pathways during early imbibition of Sisymbrium officinale L. seeds. J Exp Bot 60(6):1645–1661

    Article  PubMed  CAS  Google Scholar 

  • Iglesias-Fernández R, Matilla A (2010) Genes involved in ethylene and gibberellins metabolism are required for endosperm-limited germination of Sisymbrium officinale L. seeds. Planta 231(3):653–664

    Article  PubMed  CAS  Google Scholar 

  • Iglesias-Fernández R, Rodríguez-Gacio M, Barrero-Sicilia C, Carbonero P, Matilla A (2011) Three endo-β-mannanase genes expressed in the micropylar endosperm and in the radicle influence germination of Arabidopsis thaliana seeds. Planta 233(1):25–36

    Article  PubMed  CAS  Google Scholar 

  • Kanai M, Nishimura M, Hayashi M (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J 62(6):936–947

    PubMed  CAS  Google Scholar 

  • Kang J-H, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18(11):3303–3320

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125(1):66–71

    Article  Google Scholar 

  • Karssen CM, Zagorski S, Kepczynski J, Groot SPC (1989) Key role for endogenous gibberellins in the control of seed germination. Ann Bot 63(1):71–80

    CAS  Google Scholar 

  • Kendall SL, Hellwege A, Marriot P, Whalley C, Graham IA, Penfield S (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell Online 23(7):2568–2580

    Article  CAS  Google Scholar 

  • Klee HJ, Clark DG (2004) Ethylene signal transduction in fruits and flowers. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action. Cluver Academic, London, pp 377–398

    Google Scholar 

  • Knoester M, van Loon LC, van den Heuvel J, Hennig J, Bol JF, Linthorst HJM (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc Natl Acad Sci USA 95(4):1933–1937

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M (2002) Seed dormancy and germination. Curr Opin Plant Biol 5(1):33–36

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M, Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh. TAG Theor Appl Genet 58(6):257–263

    Article  Google Scholar 

  • Krock B, Schmidt S, Hertweck C, Baldwin IT (2002) Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual, Nicotiana attenuata. Seed Sci Res 12(04):239–252

    Article  CAS  Google Scholar 

  • Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15(04):281–307

    Article  CAS  Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16(5):646–658

    Article  PubMed  CAS  Google Scholar 

  • Leubner-Metzger G (2002) Seed after-ripening and over-expression of class I ß-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215(6):959–968

    Article  PubMed  CAS  Google Scholar 

  • Leubner-Metzger G (2003) Functions and regulation of β-1,3-glucanases during seed germination, dormancy release and after-ripening. Seed Science Research 13(01):17–34

    Article  CAS  Google Scholar 

  • Leubner-Metzger G, Meins F (2000) Sense transformation reveals a novel role for class I β-1,3-glucanase in tobacco seed germination. Plant J 23(2):215–221

    Article  PubMed  CAS  Google Scholar 

  • Leubner-Metzger G, Frundt C, Vogeli-Lange R, Meins F Jr (1995) Class I β-1,3-glucanases in the endosperm of tobacco during germination. Plant Physiol 109(3):751–759

    PubMed  CAS  Google Scholar 

  • Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vögeli-Lange R, Meins F (1998) Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I β-1,3-glucanase during tobacco seed germination. Plant Mol Biol 38(5):785–795

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60(12):3311–3336

    Article  PubMed  CAS  Google Scholar 

  • Linkies A, Müller K, Morris K, Tureckova V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, Leubner-Metzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822

    Article  PubMed  CAS  Google Scholar 

  • Linkies A, Gräber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytol 186(4):817–831

    Article  PubMed  CAS  Google Scholar 

  • Liu P–P, Koizuka N, Homrichhausen TM, Hewitt JR, Martin RC, Nonogaki H (2005) Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. Plant J 41(6):936–944

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8(5):532–540

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15(1):165–178

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16(7):1938–1950

    Article  PubMed  CAS  Google Scholar 

  • Matilla AJ (1996) Polyamines and seed germination. Seed Sci Res 6(03):81–93

    Article  CAS  Google Scholar 

  • Matilla AJ (2000) Ethylene in seed formation and germination. Seed Sci Res 10(02):111–126

    CAS  Google Scholar 

  • Matilla AJ, Matilla-Vázquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175(1–2):87–97

    Article  CAS  Google Scholar 

  • McKibbin RS, Wilkinson MD, Bailey PC, Flintham JE, Andrew LM, Lazzeri PA, Gale MD, Lenton JR, Holdsworth MJ (2002) Transcripts of Vp-1 homeologues are misspliced in modern wheat and ancestral species. Proc Natl Acad Sci 99(15):10203–10208

    Article  PubMed  CAS  Google Scholar 

  • Miersch O, Neumerkel J, Dippe M, Stenzel I, Wasternack C (2008) Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytol 177(1):114–127

    PubMed  CAS  Google Scholar 

  • Morris K, Linkies A, Müller K, Oracz K, Wang X, Lynn JR, Leubner-Metzger G, Finch-Savage WE (2011) Regulation of seed germination in the close Arabidopsis relative Lepidium sativum: a global tissue-specific transcript analysis. Plant Physiol 155(4):1851–1870

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47(7):864–877

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G (2009a) The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol 184(4):885–897

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Linkies A, Vreeburg RAM, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009b) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150(4):1855–1865

    Article  PubMed  CAS  Google Scholar 

  • Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41(5):697–709

    Article  PubMed  CAS  Google Scholar 

  • Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220(2):412–423

    Article  PubMed  CAS  Google Scholar 

  • Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20(02):55–67

    Article  CAS  Google Scholar 

  • Narsai R, Law SR, Carrie C, Xu L, Whelan J (2011) In depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis thaliana. Plant Physiol. doi:10.1104/pp.111.183129

  • Nascimento WM, Cantliffe DJ, Huber DJ (2000a) Endo-β-mannanase activity during lettuce seed germination at high temperature conditions. Acta Hortic 517:107–112

    Google Scholar 

  • Nascimento WM, Cantliffe DJ, Huber DJ (2000b) Thermotolerance in lettuce seeds: association with ethylene and endo-β-mannanase. J Am Soc Hortic Sci 125:518–524

    CAS  Google Scholar 

  • Nascimento WM, Cantliffe DJ, Huber DJ (2001) Endo-β-mannanase activity and seed germination of thermosensitive and thermotolerant lettuce genotypes in response to seed priming. Seed Sci Res 11(03):255–264

    CAS  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126(3):467–475

    Article  PubMed  CAS  Google Scholar 

  • Ni BR, Bradford KJ (1993) Germination and dormancy of abscisic acid- and gibberellin-deficient mutant tomato (Lycopersicon esculentum) seeds (sensitivity of germination to abscisic acid, gibberellin, and water potential). Plant Physiol 101(2):607–617

    PubMed  CAS  Google Scholar 

  • Nonogaki H (2006) Seed germination—the biochemical and molecular mechanisms. Breed Sci 56:93–105

    Google Scholar 

  • Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific endo ß-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiol 123:1235–1246

    Article  PubMed  CAS  Google Scholar 

  • Nonogaki H, Chen F, Bradford KJ (2007) Mechanisms and genes involved in germination sensu stricto. In: Annual plant reviews: seed development, dormancy and germination, vol 27. Blackwell Publishing Ltd

  • Norastehnia A, Sajedi RH, Nojavan-Asghari M (2007) Inhibitory effects of methyl jasmonate on seed germination in maize (Zea mays): effect on α-amylase activity and ethylene production. Gen Appl Plant Physiol 33(1–2):13–23

    CAS  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  PubMed  CAS  Google Scholar 

  • Oh E, Kang H, Yamaguchi S, Park J, Lee D, Kamiya Y, Choi G (2009) Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21(2):403–419

    Article  PubMed  CAS  Google Scholar 

  • Onkokesung N, Baldwin IT, Gális I (2010) The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores. Plant Signal Behav 5(10):1305–1307

    Article  PubMed  CAS  Google Scholar 

  • Ooms J, Leon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana (a comparative study using abscisic acid-insensitive abi3 mutants). Plant Physiol 102(4):1185–1191

    PubMed  CAS  Google Scholar 

  • Oracz K, Voegele A, Tarkowská D, Jacquemoud D, Turecková V, Urbanová D, Strnad M, Sliwinska E, Leubner-Metzger G (2011) Myrigalone A inhibits Lepidium sativum seed germination by interference with gibberellin metabolism and apoplastic superoxide production required for embryo extension growth and endosperm rupture. Plant Cell Physiol, in press

  • Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase. Planta 211(1):144–149

    Article  PubMed  CAS  Google Scholar 

  • Petruzzelli L, Müller K, Hermann K, Leubner-Metzger G (2003a) Distinct expression patterns of ß-1,3-glucanases and chitinases during the germination of Solanaceous seeds. Seed Sci Res 13:139–153

    Article  CAS  Google Scholar 

  • Petruzzelli L, Sturaro M, Mainieri D, Leubner-Metzger G (2003b) Calcium requirement for ethylene-dependent responses involving 1-aminocyclopropane-1-carboxylic acid oxidase in radicle tissues of germinated pea seeds. Plant Cell Environ 26(5):661–671

    Article  CAS  Google Scholar 

  • Pinfield-Wells H, Rylott EL, Gilday AD, Graham S, Job K, Larson TR, Graham IA (2005) Sucrose rescues seedling establishment but not germination of Arabidopsis mutants disrupted in peroxisomal fatty acid catabolism. Plant J 43(6):861–872

    Article  PubMed  CAS  Google Scholar 

  • Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20(10):2729–2745

    Article  PubMed  CAS  Google Scholar 

  • Porta H, Rueda-Benítez P, Campos F, Colmenero-Flores JM, Colorado JM, Carmona MJ, Covarrubias AA, Rocha-Sosa M (1999) Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant Cell Physiol 40(8):850–858

    PubMed  CAS  Google Scholar 

  • Preston CA, Betts H, Baldwin IT (2002) Methyl jasmonate as an allelopathic agent: sagebrush inhibits germination of a neighboring tobacco Nicotiana Attenuata. J Chem Ecol 28(11):2343–2369

    Article  PubMed  CAS  Google Scholar 

  • Preston J, Tatematsu K, Kanno Y, Hobo T, Kimura M, Jikumaru Y, Yano R, Kamiya Y, Nambara E (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell Physiol 50(10):1786–1800

    Article  PubMed  CAS  Google Scholar 

  • Pritchard SL, Charlton WL, Baker A, Graham IA (2002) Germination and storage reserve mobilization are regulated independently in Arabidopsis. Plant J 31(5):639–647

    Article  PubMed  CAS  Google Scholar 

  • Quettier A-L, Shaw E, Eastmond PJ (2008) SUGAR-DEPENDENT6 encodes a mitochondrial flavin adenine dinucleotide-dependent glycerol-3-P dehydrogenase, which is required for glycerol catabolism and postgerminative seedling growth in Arabidopsis. Plant Physiol 148(1):519–528

    Article  PubMed  CAS  Google Scholar 

  • Rentzsch S, Podzimska D, Voegele A, Imbeck M, Müller K, Linkies A, Leubner-Metzger G (2011) Dose- and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of α-amylases and β-amylases. Planta:1–15. doi:10.1007/s00425-011-1501-1

  • Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58(15–16):4047–4060

    Article  PubMed  CAS  Google Scholar 

  • Rojo E, León J, Sánchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20(2):135–142

    Article  PubMed  CAS  Google Scholar 

  • Rojo E, Solano R, Sánchez-Serrano J (2003) Interactions between signaling compounds involved in plant defense. J Plant Growth Regul 22(1):82–98

    Article  CAS  Google Scholar 

  • Romanel EA, Schrago CG, Counago RM, Russo CA, Alves-Ferreira M (2009) Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PloS one 4 (6): doi:10.1371/journal.pone.0005791

  • Russell L, Larner V, Kurup S, Bougourd S, Holdsworth M (2000) The Arabidopsis COMATOSE locus regulates germination potential. Development 127(17):3759–3767

    PubMed  CAS  Google Scholar 

  • Sargent JA, Osborne DJ (1980) A comparative study of the fine structure of coleorhiza and root cells during the early hours of germination of rye embryos. Protoplasma 104(1):91–103

    Article  Google Scholar 

  • Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125(4):1591–1602

    Article  PubMed  CAS  Google Scholar 

  • Schwachtje J, Baldwin IT (2004) Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata. Seed Sci Res 14(01):51–60

    Article  CAS  Google Scholar 

  • Siriwitayawan G, Geneve RL, Bruce Downie A (2003) Seed germination of ethylene perception mutants of tomato and Arabidopsis. Seed Sci Res 13(04):303–314

    Article  CAS  Google Scholar 

  • Sliwinska E, Bassel GW, Bewley JD (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. J Exp Bot 60(12):3587–3594

    Article  PubMed  CAS  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12(23):3703–3714

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16(8):2117–2127

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89(15):6837–6840

    Article  PubMed  CAS  Google Scholar 

  • Staswick P, Tiryaki I, Rowe ML (2002) Jasmonate Response Locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14(6):1405–1415

    Article  PubMed  CAS  Google Scholar 

  • Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, Reski R, Feussner I (2010) The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol 188(3):740–749

    Article  PubMed  CAS  Google Scholar 

  • Suza W, Staswick P (2008) The role of JAR1 in Jasmonoyl-l-isoleucine production during Arabidopsis wound response. Planta 227(6):1221–1232

    Article  PubMed  CAS  Google Scholar 

  • Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124(4):437–453

    Article  PubMed  CAS  Google Scholar 

  • Teng S, Rognoni S, Bentsink L, Smeekens S (2008) The Arabidopsis GSQ5/DOG1 Cvi allele is induced by the ABA-mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating ABI4 expression. Plant J 55(3):372–381

    Article  PubMed  CAS  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448(7154):661–665

    Article  PubMed  CAS  Google Scholar 

  • Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Aso Y, Ishiyama K, Tamura N, Iuchi S, Kobayashi M, Yamaguchi S, Kamiya Y, Nambara E, Kawakami N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146(3):1368–1385

    Article  PubMed  CAS  Google Scholar 

  • Toorop PE, van Aelst AC, Hilhorst HWM (2000) The second step of the biphasic endosperm cap weakening that mediates tomato (Lycopersicon esculentum) seed germination is under control of ABA. J Exp Bot 51(349):1371–1379

    Article  PubMed  CAS  Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-Northerns, Expression Angling, and promoter analyses. Plant J 43(1):153–163

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche F, Fierro A, Wiedemann G, Reski R, Van Der Straeten D (2007) Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biol 7(1):65–81

    Article  PubMed  CAS  Google Scholar 

  • Vick BA, Zimmerman DC (1983) The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem Biophys Res Commun 111(2):470–477

    Article  PubMed  CAS  Google Scholar 

  • Vijayan P, Shockey J, Lévesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95(12):7209–7214

    Article  PubMed  CAS  Google Scholar 

  • Voegele A, Linkies A, Müller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot. doi:10.1093/jxb/err214

  • Walne PL, Haber AH, Triplett LL (1975) Ultrastructure of auxin-induced tumors of the coleorhiza-epiblast of wheat. Am J Bot 62(1):58–66

    Article  CAS  Google Scholar 

  • Wang A, Li J, Bewley JD (2004) Molecular cloning and characterization of an endo-β-mannanase gene expressed in the lettuce endosperm following radicle emergence. Seed Sci Res 14(03):267–276

    Article  CAS  Google Scholar 

  • Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proceedings of the National Academy of Sciences 106(10):3853–3858

    Article  CAS  Google Scholar 

  • Wasternack C (2004) Jasmonates—biosynthesis and role in stress responses and developmental processes. Plant cell death processes. Elsevier, New York

    Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C, Kombrink E (2009) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5(1):63–77

    Article  CAS  Google Scholar 

  • Watt MS, Bloomberg M, Finch-Savage WE (2011) Development of a hydrothermal time model that accurately characterises how thermoinhibition regulates seed germination. Plant Cell Environ 34(5):870–876

    Article  PubMed  CAS  Google Scholar 

  • Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62(10):3289–3309

    Article  PubMed  CAS  Google Scholar 

  • Wilen RW, van Rooijen GJH, Pearce DW, Pharis RP, Holbrook LA, Moloney MM (1991) Effects of jasmonic acid on embryo-specific processes in Brassica and Linum oilseeds. Plant Physiol 95(2):399–405

    Article  PubMed  CAS  Google Scholar 

  • Wu C-T, Bradford KJ (2003) Class I chitinase and β-1,3-glucanase are differentially regulated by wounding, methyl jasmonate, ethylene, and gibberellin in tomato seeds and leaves. Plant Physiol 133(1):263–273

    Article  PubMed  CAS  Google Scholar 

  • Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280(5366):1091–1094

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6(8):1077–1085

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D (2002) The SCFCOI1 ubiquitin–ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14(8):1919–1935

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16(2):367–378

    Article  PubMed  CAS  Google Scholar 

  • Yan Y, Stolz S, Chételat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19(8):2470–2483

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 Protein is a jasmonate receptor. Plant Cell 21(8):2220–2236

    Article  PubMed  CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35(1):155–189

    Article  CAS  Google Scholar 

  • Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17(14):1225–1230

    Article  PubMed  CAS  Google Scholar 

  • Zalewski K, Nitkiewicz B, Lahuta LB, Glowacka K, Socha A, Amarowicz R (2010) Effect of jasmonic acid-methyl ester on the composition of carbohydrates and germination of yellow lupine (Lupinus luteus L.) seeds. J Plant Physiol 167(12):967–973

    Article  PubMed  CAS  Google Scholar 

  • Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP (2002) Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416(6882):703–709

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Our work and the position of A.L. are funded by the Deutsche Forschungsgemeinschaft (Grant No. DFG Le720/6), which is gratefully acknowledged.

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Linkies, A., Leubner-Metzger, G. Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31, 253–270 (2012). https://doi.org/10.1007/s00299-011-1180-1

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