Molecular and Hormonal Regulation of Thermoinhibition of Seed Germination

Chapter

Abstract

Thermoinhibition is the failure of seeds to germinate when imbibed at warm but not excessively high temperatures. Such seeds can generally complete germination when the temperature is reduced, but extended exposure to high temperatures may induce secondary dormancy. Plant hormones, particularly abscisic acid (ABA), gibberellins (GA) and ethylene, are known to be involved in regulating thermoinhibition of germination. Key regulated genes involved in ABA biosynthesis such as those encoding 9-cis-EPOXYCAROTENOID DIOXYGENASE (NCEDs) are essential for the induction of thermoinhibition. GA and ethylene biosynthetic and signaling genes are associated with promotion of germination and are repressed in thermoinhibited seeds. Jasmonates, strigolactones and other stress-related genes/proteins may also contribute to temperature regulation of germination, possibly by affecting ABA, GA or ethylene synthesis or action. The molecular biology and physiology of these genes and hormones and their interactions are described along with directions for future research into the temperature regulation of seed germination.

Keywords

Seed Germination Temperature Thermoinhibition Dormancy Gene expression Abscisic acid (ABA) Gibberellin (GA) Ethylene Jasmonate Strigolactone Heat shock Stress 

References

  1. Alia, Hayashi H, Sakamoto A, Murata N (1998) Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J 16:155–161PubMedGoogle Scholar
  2. Allen PS, Benech-Arnold RL, Batlla D, Bradford KJ (2007) Modeling of seed dormancy. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell Publishing, Oxford, pp 72–112Google Scholar
  3. Alonso-Blanco C, Bentsink L, Hanhart CJ, Blankestijn-de Vries H, Koornneef M (2003) Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164:711–729PubMedCentralPubMedGoogle Scholar
  4. Alvarado V, Bradford KJ (2002) A hydrothermal time model explains the cardinal temperatures for seed germination. Plant Cell Environ 25:1061–1069Google Scholar
  5. Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63PubMedCentralPubMedGoogle Scholar
  6. 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 148:926–947PubMedCentralPubMedGoogle Scholar
  7. Argyris J, Truco MJ, Ochoa O, McHale L, Dahal P, Van Deynze A et al (2011) A gene encoding an abscisic acid biosynthetic enzyme (LsNCED4) collocates with the high temperature germination locus Htg6.1 in lettuce (Lactuca sp.). Theor Appl Genet 122:95–108PubMedCentralPubMedGoogle Scholar
  8. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321PubMedGoogle Scholar
  9. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, New YorkGoogle Scholar
  10. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115PubMedCentralPubMedGoogle Scholar
  11. Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci U S A 103:17042–17047PubMedCentralPubMedGoogle Scholar
  12. Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New YorkGoogle Scholar
  13. Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18PubMedGoogle Scholar
  14. Bogatek R, Gniazdowska A (2012) Ethylene in seed development, dormancy and germination. In: McManus MT (ed) Annual plant reviews 44. Blackwell Publishing Ltd., Oxford, pp 189–218Google Scholar
  15. Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 46:805–822PubMedGoogle Scholar
  16. Cantliffe DJ, Sung Y, Nascimento WM (2000) Lettuce seed germination. Hortic Rev 224:229–275Google Scholar
  17. Carter AK, Stevens R (1998) Using ethephon and GA3 to overcome thermoinhibition in ‘Jalapeño M’ pepper seed. HortScience 33:1026–1027Google Scholar
  18. Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35:1912–1931PubMedGoogle Scholar
  19. Chen MX, Wang Z, Zhu YN, Li ZL, Hussain N, Xuan LJ et al (2012) The effect of TRANSPARENT TESTA2 on seed fatty acid biosynthesis and tolerance to environmental stresses during young seedling establishment in Arabidopsis. Plant Physiol 160:1023–1036PubMedCentralPubMedGoogle Scholar
  20. Cheng WH, Chiang MH, Hwang SG, Lin PC (2009) Antagonism between abscisic acid and ethylene in Arabidopsis acts in parallel with the reciprocal regulation of their metabolism and signaling pathways. Plant Mol Biol 71:61–80PubMedCentralPubMedGoogle Scholar
  21. Chiang GCK, Bartsch M, Barua D, Nakabayashi K, Debieu M, Kronholm I et al (2011) DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol Ecol 20:3336–3349PubMedGoogle Scholar
  22. Chiu RS, Nahal H, Provart NJ, Gazzarrini S (2012) The role of the Arabidopsis FUSCA3 transcription factor during inhibition of seed germination at high temperature. BMC Plant Biol 12:15PubMedCentralPubMedGoogle Scholar
  23. Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS et al (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 42:35–48PubMedGoogle Scholar
  24. Chono M, Honda I, Shinoda S, Kushiro T, Kamiya Y, Nambara E et al (2006) Field studies on the regulation of abscisic acid content and germinability during grain development of barley: molecular and chemical analysis of pre-harvest sprouting. J Exp Bot 57:2421–2434PubMedGoogle Scholar
  25. Contreras S, Bennett MA, Tay D (2009) Temperature during seed development affects weight, germinability and storability of lettuce seeds. Seed Sci Technol 37:398–412Google Scholar
  26. Corbineau F, Rudnicki R, Come D (1988) Induction of secondary dormancy in sunflower seeds by high temperature. Possible involvement of ethylene biosynthesis. Physiol Plant 73:368–373Google Scholar
  27. Covell S, Ellis RH, Roberts EH, Summerfield RJ (1986) The influence of temperature on seed germination rate in grain legumes. 1. A comparison of chickpea, lentil, soybean and cowpea at constant temperatures. J Exp Bot 37:705–715Google Scholar
  28. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679PubMedGoogle Scholar
  29. Dave A, Hernandez ML, He Z, Andriotis VM, Vaistij FE, Larson TR et al (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599PubMedCentralPubMedGoogle Scholar
  30. Debeaujon I, Koornneef M (2000) Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol 122:415–424PubMedCentralPubMedGoogle Scholar
  31. Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–413PubMedCentralPubMedGoogle Scholar
  32. Donohue K (2014) Why ontogeny matters during adaptation: developmental niche construction and pleiotropy across the life cycle in Arabidopsis thaliana. Evolution 68:32–47PubMedGoogle Scholar
  33. Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319Google Scholar
  34. Downie AB, Zhang D, Dirk LM, Thacker RR, Pfeiffer JA, Drake JL et al (2003) Communication between the maternal testa and the embryo and/or endosperm affect testa attributes in tomato. Plant Physiol 133:145–160PubMedCentralPubMedGoogle Scholar
  35. Dutta S, Bradford KJ (1994) Water relations of lettuce seed thermoinhibition. II. Ethylene and endosperm effects on base water potential. Seed Sci Res 4:11–18Google Scholar
  36. Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5:765–771Google Scholar
  37. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609PubMedCentralPubMedGoogle Scholar
  38. Finkelstein RR, Somerville CR (1990) Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol 94:1172–1179PubMedCentralPubMedGoogle Scholar
  39. Foley ME, Chao WS, Horvath DP, Dogramaci M, Anderson JV (2013) The transcriptomes of dormant leafy spurge seeds under alternating temperature are differentially affected by a germination-enhancing pretreatment. J Plant Physiol 170:539–547PubMedGoogle Scholar
  40. Fonseca S, Chico JM, Solano R (2009) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12:539–547PubMedGoogle Scholar
  41. Footitt S, Huang Z, Clay HA, Mead A, Finch-Savage WE (2013) Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. Plant J 74:1003–1015PubMedCentralPubMedGoogle Scholar
  42. Franklin KA, Wigge PA (eds) (2014) Temperature and plant development. Wiley, AmesGoogle Scholar
  43. Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol Appl 7:123–139PubMedCentralPubMedGoogle Scholar
  44. Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A et al (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70:501–512PubMedGoogle Scholar
  45. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY et al (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–U138PubMedCentralPubMedGoogle Scholar
  46. Gabriele S, Rizza A, Martone J, Circelli P, Costantino P, Vittorioso P (2010) The Dof protein DAG1 mediates PIL5 activity on seed germination by negatively regulating GA biosynthetic gene AtGA3ox1. Plant J 61:312–323PubMedGoogle Scholar
  47. Gallardo M, Delgado MD, Sanchezcalle IM, Matilla AJ (1991) Ethylene production and 1-aminocyclopropane-1-carboxylic acid conjugation in thermoinhibited Cicer arietinum L. seeds. Plant Physiol 97:122–127PubMedCentralPubMedGoogle Scholar
  48. Gallardo M, Derueda PM, Matilla A, Sanchezcalle IM (1994) The relationships between ethylene production and germination of Cicer arietinum Seeds. Biologia Plantarum 36:201–207Google Scholar
  49. 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 12:1117–1126PubMedCentralPubMedGoogle Scholar
  50. Gonai T, Kawahara S, Tougou M, Satoh S, Hashiba T, Hirai N et al (2004) Abscisic acid in the thermoinhibition of lettuce seed germination and enhancement of its catabolism by gibberellin. J Exp Bot 55:111–118PubMedGoogle Scholar
  51. Gonzalez-Guzman M, Apostolova N, Belles JM, Barrero JM, Piqueras P, Ponce MR et al (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14:1833–1846PubMedCentralPubMedGoogle Scholar
  52. Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35:1769–1786PubMedGoogle Scholar
  53. Graeber K, Linkies A, Steinbrecher T, Mummenhoff K, Tarkowská D, Turečková V et al (2014) DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination. Proc Natl Acad Sci U S A 10:1073/pnas.1403851111Google Scholar
  54. Grasser M, Kane CM, Merkle T, Melzer M, Emmersen J, Grasser KD (2009) Transcript elongation factor TFIIS is involved in Arabidopsis seed dormancy. J Mol Biol 386:598–611PubMedGoogle Scholar
  55. Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414PubMedCentralPubMedGoogle Scholar
  56. Guedes AC, Cantliffe DJ (1980) Germination of lettuce seeds at high temperature after seed priming. J Am Soc Hortic Sci 105:777–781Google Scholar
  57. Harrington JD, Thompson RC (1952) Effect of variety and area of production on subsequent germination of lettuce seed at high temperatures. Proc Am Soc Hortic Sci 59:445–450Google Scholar
  58. Hayashi E, Aoyama N, Still DW (2008) Quantitative trait loci associated with lettuce seed germination under different temperature and light environments. Genome 51:928–947PubMedGoogle Scholar
  59. Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Hess B et al (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 58:3047–3060PubMedGoogle Scholar
  60. Hilhorst HWM (2007) Definitions and hypotheses of seed dormancy. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell Publishing, Oxford, pp 50–71Google Scholar
  61. Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54PubMedGoogle Scholar
  62. Huang XL, Khan AA (1992) Alleviation of thermoinhibition in preconditioned lettuce seeds involves ethylene, not polyamine biosynthesis. J Am Soc Hortic Sci 117:841–845Google Scholar
  63. Huang D, Koh C, Feurtado JA, Tsang EW, Cutler AJ (2013) MicroRNAs and their putative targets in Brassica napus seed maturation. BMC Genomics 14:140PubMedCentralPubMedGoogle Scholar
  64. Huo H, Dahal P, Kunusoth K, McCallum CM, Bradford KJ (2013) Expression of 9-cis-EPOXYCAROTENOID DIOXYGENASE4 is essential for thermoinhibition of lettuce seed germination but not for seed development or stress tolerance. Plant Cell 25:884–900PubMedCentralPubMedGoogle Scholar
  65. Iglesias-Fernandez R, Matilla AJ (2010) Genes involved in ethylene and gibberellins metabolism are required for endosperm-limited germination of Sisymbrium officinale L. seeds. Planta 231:653–664PubMedGoogle Scholar
  66. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T et al (2001) Regulation of drought tolerance by gene manipulation of 9-CIS-EPOXYCAROTENOID DIOXYGENASE, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333PubMedGoogle Scholar
  67. Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896PubMedCentralPubMedGoogle Scholar
  68. Jacobsen JV, Barrero JM, Hughes T, Julkowska M, Taylor JM, Xu Q et al (2013) Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.). Planta 238:121–138PubMedGoogle Scholar
  69. 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 62:936–947PubMedGoogle Scholar
  70. 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 23:2568–25580PubMedCentralPubMedGoogle Scholar
  71. Kepczynska E, Piekna-Grochala J, Kepczynski J (2006) Hormonal regulation of tomato seed germination at a supraoptimal temperature. Acta Physiol Plant 28:225–231Google Scholar
  72. Kepczynski J, Bihun M (2002) Induction of secondary dormancy in Amaranthus caudatus seeds. Plant Growth Regul 38:135–140Google Scholar
  73. Kepczynski J, Kepczynska E (1997) Ethylene in seed dormancy and germination. Physiol Plant 101:720–726Google Scholar
  74. Kepczynski J, Bihun M, Kepczynska E (2006) Implication of ethylene in the release of secondary dormancy in Amaranthus caudatus L. seeds by gibberellins or cytokinin. Plant Growth Regul 48:119–126Google Scholar
  75. Khan AA, Huang XL (1987) Synergistic promotion of ethylene production and germination by cytokinin and ACC in lettuce seeds exposed to high-temperature and salinity stress. HortScience 22:1126Google Scholar
  76. Khan AA, Prusinski J (1989) Kinetin enhanced 1-aminocyclopropane-1-carboxylic acid utilization during alleviation of high temperatures stress in lettuce seeds. Plant Physiol 91:733–737PubMedCentralPubMedGoogle Scholar
  77. Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A et al (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20:1260–1277PubMedCentralPubMedGoogle Scholar
  78. Kimball S, Angert AL, Huxman TE, Venable DL (2011) Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran desert winter annuals Am J Bot 98:1773–1781PubMedGoogle Scholar
  79. Koornneef M, Jorna ML (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Henyh. Theor Appl Genet 61:385–393PubMedGoogle Scholar
  80. Koornneef M, Vanderveen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L) Heynh. Theor Appl Genet 58:257–263PubMedGoogle Scholar
  81. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383Google Scholar
  82. Korkmaz A (2006) Ameliorative effects of ethylene precursor and polyamines on the high temperature inhibition of seed germination in lettuce (Lactuca sativa L.) before and after seed storage. Seed Sci Technol 34:465–474Google Scholar
  83. Kozarewa I, Cantliffe DJ, Nagata RT, Stoffella PJ (2006) High maturation temperature of lettuce seeds during development increased ethylene production and germination at elevated temperatures. J Am Soc Hortic Sci 131:564–570Google Scholar
  84. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T et al (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656PubMedCentralPubMedGoogle Scholar
  85. Lafta A, Mou BQ (2013) Evaluation of lettuce genotypes for seed thermotolerance. HortScience 48:708–714Google Scholar
  86. Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748PubMedGoogle Scholar
  87. Lee SC, Cheng H, King KE, Wang WF, He YW, Hussain A et al (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658PubMedCentralPubMedGoogle Scholar
  88. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M et al (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45:309–319PubMedGoogle Scholar
  89. Lei L, Zhu X, Wang S, Zhu M, Carver BF, Yan L (2013) TaMFT-A1 is associated with seed germination sensitive to temperature in winter wheat. PLoS One 8:e73330PubMedCentralPubMedGoogle Scholar
  90. Leon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH et al (1996a) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661PubMedGoogle Scholar
  91. Leon-Kloosterziel KM, van de Bunt GA, Zeevaart JA, Koornneef M (1996b) Arabidopsis mutants with a reduced seed dormancy. Plant Physiol 110:233–240PubMedCentralPubMedGoogle Scholar
  92. Leubner-Metzger G (2002) Seed after-ripening and over-expression of class I β-1, 3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215:959–968PubMedGoogle Scholar
  93. Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vogeli-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 38:785–795PubMedGoogle Scholar
  94. Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771PubMedCentralPubMedGoogle Scholar
  95. Leymarie J, Robayo-Romero ME, Gendreau E, Benech-Arnold RL, Corbineau F (2008) Involvement of ABA in induction of secondary dormancy in barley (Hordeum vulgare L.) seeds. Plant Cell Physiol 49:1830–1838PubMedGoogle Scholar
  96. Li S, Li F, Wang J, Zhang W, Meng Q, Chen TH et al (2011) Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant Cell Environ 34:1931–1943PubMedGoogle Scholar
  97. Lim S, Park J, Lee N, Jeong J, Toh S, Watanabe A et al (2013) ABA-INSENSITIVE3, ABA-INSENSITIVE5, and DELLAs interact to activate the expression of SOMNUS and other high-temperature-inducible genes in imbibed seeds in Arabidopsis. Plant Cell 25:4863–4878PubMedCentralPubMedGoogle Scholar
  98. Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, Cheng WH (2007) Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143:745–758PubMedCentralPubMedGoogle Scholar
  99. Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270PubMedGoogle Scholar
  100. Linkies A, Muller K, Morris K, Tureckova V, Wenk M, Cadman CSC et al (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822PubMedCentralPubMedGoogle Scholar
  101. Liu YX, Koornneef M, Soppe WJJ (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19:433–444PubMedCentralPubMedGoogle Scholar
  102. Liu Y, Geyer R, van Zanten M, Carles A, Li Y, Horold A et al (2011) Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. Plos One 6:e22241PubMedCentralPubMedGoogle Scholar
  103. Long SP, Ort DR (2010) More than taking the heat: crops and global change. Curr Opin Plant Biol 13:241–248PubMedGoogle Scholar
  104. Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci U S A 98:4782–1787PubMedCentralPubMedGoogle Scholar
  105. Lopez-Molina L, Mongrand B, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328PubMedGoogle Scholar
  106. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A et al (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  107. Machabee S, Saini HS (1991) Differences in the requirement for endogenous ethylene during germination of dormant and nondormant seeds of Chenopodium album L. J Plant Physiol 138:97–101Google Scholar
  108. Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P et al (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15:2331–2342PubMedCentralPubMedGoogle Scholar
  109. Martinez-Andújar C, Ordiz MI, Huang Z, Nonogaki M, Beachy RN, Nonogaki H (2011) Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proc Natl Acad Sci U S A 108:17225–17229PubMedCentralPubMedGoogle Scholar
  110. Martínez-Andújar C, Pluskota WE, Bassel GW, Asahina M, Pupel P, Nguyen TT et al (2012) Mechanisms of hormonal regulation of endosperm cap-specific gene expression in tomato seeds. Plant J 71:575–586PubMedGoogle Scholar
  111. Matilla AJ, Matilla-Vazquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–97Google Scholar
  112. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP et al (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130PubMedCentralPubMedGoogle Scholar
  113. Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560PubMedGoogle Scholar
  114. Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T et al (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818PubMedGoogle Scholar
  115. Mortensen SA, Sonderkaer M, Lynggaard C, Grasser M, Nielsen KL, Grasser KD (2011) Reduced expression of the DOG1 gene in Arabidopsis mutant seeds lacking the transcript elongation factor TFIIS. FEBS Lett 585:1929–1933PubMedGoogle Scholar
  116. Nakabayashi K, Bartsch M, Xiang Y, Miatton E, Pellengahr S, Yano R et al (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell 24:2826–2838PubMedCentralPubMedGoogle Scholar
  117. Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889PubMedGoogle Scholar
  118. Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T et al (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229PubMedCentralPubMedGoogle Scholar
  119. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185PubMedGoogle Scholar
  120. 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 20:55–67Google Scholar
  121. Nascimento WM, Cantliffe DJ, Huber DJ (2000) Thermotolerance in lettuce seeds: association with ethylene and endo-β-mannanase. J Am Soc Hortic Sci 125:518–524Google Scholar
  122. 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 11:255–264Google Scholar
  123. Nascimento WM, Cantliffe DJ, Huber DJ (2004) Ethylene evolution and endo-β-mannanase activity during lettuce seed germination at high temperature. Sci Agric 61:156–163Google Scholar
  124. Nascimento WM, Vieira JV, Silva GO, Reitsma KR, Cantliffe DJ (2008) Carrot seed germination at high temperature: effect of genotype and association with ethylene production. HortScience 43:1538–1543Google Scholar
  125. Nascimento WM, Huber DJ, Cantliffe DJ (2013) Carrot seed germination and respiration at high temperature in response to seed maturity and priming. Seed Sci Technol 41:164–169Google Scholar
  126. Nonogaki H (2010) MicroRNA gene regulation cascades during early stages of plant development. Plant Cell Physiol 51:1840–1846PubMedGoogle Scholar
  127. Nonogaki H (2014) Seed dormancy and germination—Emerging mechanisms and new hypotheses. Front Plant Science 5:233Google Scholar
  128. Ogawa M, Hanada A, Yamauchi Y, Kuwalhara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604PubMedCentralPubMedGoogle Scholar
  129. Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I et al (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19:1192–1208PubMedCentralPubMedGoogle Scholar
  130. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N et al (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107PubMedCentralPubMedGoogle Scholar
  131. Papi M, Sabatini S, Altamura MM, Hennig L, Schafer E, Costantino P et al (2002) Inactivation of the phloem-specific dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol 128:411–417PubMedCentralPubMedGoogle Scholar
  132. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedCentralPubMedGoogle Scholar
  133. Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628PubMedGoogle Scholar
  134. Penfield S, MacGregor D (2014) Temperature sensing in plants. In: Franklin KA, Wigge PA (eds) Temperature and plant development. Wiley Blackwell, Oxford, pp 1–18Google Scholar
  135. Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclopropane-1-carboxylic acid oxidase. Planta 211:144–149PubMedGoogle Scholar
  136. Pinfield-Wells H, Rylott EL, Gilday AD, Graham S, Job K, Larson TR et al (2005) Sucrose rescues seedling establishment but not germination of Arabidopsis mutants disrupted in peroxisomal fatty acid catabolism. Plant J 43:861–872PubMedGoogle Scholar
  137. 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 20:2729–2745PubMedCentralPubMedGoogle Scholar
  138. Probert RJ (1992) The role of temperature in germination ecophysiology. In: Fenner M (ed) The ecology of regeneration in plant communities. CAB International, Melksham, pp 285–325Google Scholar
  139. Qin XQ, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551PubMedCentralPubMedGoogle Scholar
  140. Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LSP, Fujita Y et al (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol 157:1900–1913PubMedCentralPubMedGoogle Scholar
  141. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C et al (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533PubMedGoogle Scholar
  142. Rizza A, Boccaccini A, Lopez-Vidriero I, Costantino P, Vittorioso P (2011) Inactivation of the ELIP1 and ELIP2 genes affects Arabidopsis seed germination. New Phytol 190:896–905PubMedGoogle Scholar
  143. Russell L, Larner V, Kurup S, Bougourd S, Holdsworth M (2000) The Arabidopsis COMATOSE locus regulates germination potential. Development 127:3759–3767PubMedGoogle Scholar
  144. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83PubMedGoogle Scholar
  145. Saatkamp A, Affre L, Dutoit T, Poschlod P (2011) Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Ann Bot 107:415–426PubMedCentralPubMedGoogle Scholar
  146. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O et al (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37:354–369PubMedGoogle Scholar
  147. Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol 141:1389–1399PubMedCentralPubMedGoogle Scholar
  148. Saini HS, Consolacion ED, Bassi PK, Spencer MS (1986) Requirement for ethylene synthesis and action during relief of thermoinhibition of lettuce seed germination by combinations of gibberellic acid, kinetin, and carbon dioxide. Plant Physiol 81:950–953PubMedCentralPubMedGoogle Scholar
  149. Saini HS, Consolacion ED, Bassi PK, Spencer MS (1989) Control processes in the induction and relief of thermoinhibition of lettuce seed germination: actions of phytochrome and endogenous ethylene. Plant Physiol 90:311–315PubMedCentralPubMedGoogle Scholar
  150. Salaita L, Kar RK, Majee M, Downie AB (2005) Identification and characterization of mutants capable of rapid seed germination at 10 degrees C from activation-tagged lines of Arabidopsis thaliana. J Exp Bot 56:2059–2069PubMedGoogle Scholar
  151. Sawada Y, Aoki M, Nakaminami K, Mitsuhashi W, Tatematsu K, Kushiro T et al (2008) Phytochrome- and gibberellin-mediated regulation of abscisic acid metabolism during germination of photoblastic lettuce seeds. Plant Physiol 146:1386–1396PubMedCentralPubMedGoogle Scholar
  152. Schwartz SH, Zeevaart JAD (2010) Abscisic acid biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones-biosynthesis, signal transduction, action!, 3rd edn. Springer, Netherlands, pp 137–155Google Scholar
  153. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874PubMedGoogle Scholar
  154. Schwember AR, Bradford KJ (2010) A genetic locus and gene expression patterns associated with the priming effect on lettuce seed germination at elevated temperatures. Plant Mol Biol 73:105–118PubMedCentralPubMedGoogle Scholar
  155. Shukla RK, Tripathi V, Jain D, Yadav RK, Chattopadhyay D (2009) CAP2 enhances germination of transgenic tobacco seeds at high temperature and promotes heat stress tolerance in yeast. FEBS J 276:5252–5262PubMedGoogle Scholar
  156. Siriwitayawan G, Geneve RL, Downie AB (2003) Seed germination of ethylene perception mutants of tomato and Arabidopsis. Seed Sci Res 13:303–314Google Scholar
  157. Small JGC, Schultz C, Cronje E (1993) Relief of thermoinhibition in Grand Rapids lettuce seeds by oxygen plus kinetin and their effects on respiration, content of ethanol and ATP and synthesis of ethylene. Seed Sci Res 3:129–135Google Scholar
  158. Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1–1 in Arabidopsis thaliana. Genetics 149:509–521PubMedCentralPubMedGoogle Scholar
  159. Sun TP (2008) Gibberellin metabolism, perception and signaling pathways in Arabidopsis. Arabidopsis Book 6:e0103PubMedCentralPubMedGoogle Scholar
  160. Sung Y, Cantliffe DJ, Nagata RT (1998) Seed developmental temperature regulation of thermotolerance in lettuce. J Am Soc Hortic Sci 123:700–705Google Scholar
  161. Tamura N, Yoshida T, Tanaka A, Sasaki R, Bando A, Toh S et al (2006) Isolation and characterization of high temperature-resistant germination mutants of Arabidopsis thaliana. Plant Cell Physiol 47:1081–1094PubMedGoogle Scholar
  162. Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K et al (2003) Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family. Plant J 35:44–56PubMedGoogle Scholar
  163. Taylor NJ, Hills PN, Gold JD, Stirk WA, van Staden J (2005) Factors contributing to the regulation of thermoinhibition in Tagetes minuta L. J Plant Physiol 162:1270–1279PubMedGoogle Scholar
  164. Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385PubMedCentralPubMedGoogle Scholar
  165. Toh S, Kamiya Y, Kawakami N, Nambara E, McCourt P, Tsuchiya Y (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol 53:107–117PubMedGoogle Scholar
  166. Toyomasu T, Tsuji H, Yamane H, Nakayama M, Yamaguchi I, Murofushi N et al (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. J Plant Growth Regul 12:85–90Google Scholar
  167. Toyomasu T, Yamane H, Murofushi N, Inoue Y (1994) Effects of exogenously applied gibberellin and red light on the endogenous levels of abscisic acid in photoblastic lettuce seeds. Plant Cell Physiol 35:127–129Google Scholar
  168. Tuan PA, Park SU (2013) Molecular cloning and characterization of cDNAs encoding carotenoid cleavage dioxygenase in bitter melon (Momordica charantia). J Plant Physiol 170:115–120PubMedGoogle Scholar
  169. Tyler L, Thomas SG, Hu JH, Dill A, Alonso JM, Ecker JR et al (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019PubMedCentralPubMedGoogle Scholar
  170. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K et al (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci U S A 106:17588–17593PubMedCentralPubMedGoogle Scholar
  171. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K et al (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839PubMedCentralPubMedGoogle Scholar
  172. Valdes VM, Bradford KJ (1987) Effects of seed coating and osmotic priming on the germination of lettuce seeds. J Am Soc Hortic Sci 112:153–156Google Scholar
  173. Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161:1251–1264PubMedCentralPubMedGoogle Scholar
  174. Wang KLC, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950PubMedGoogle Scholar
  175. Wang Y, Liu C, Li K, Sun F, Hu H, Li X et al (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64:633–644PubMedGoogle Scholar
  176. Wang Y, Li L, Ye T, Zhao S, Liu Z, Feng YQ et al (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J 68:249–261PubMedGoogle Scholar
  177. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedCentralPubMedGoogle Scholar
  178. Weitbrecht K, Muller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309PubMedGoogle Scholar
  179. Wigge PA (2013) Ambient temperature signalling in plants. Curr Opin Plant Biol 16:661–666PubMedGoogle Scholar
  180. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A et al (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220PubMedCentralPubMedGoogle Scholar
  181. Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083PubMedCentralPubMedGoogle Scholar
  182. Yamaguchi S, Smith MW, Brown RGS, Kamiya Y, Sun TP (1998) Phytochrome regulation and differential expression of gibberellin 3 β-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126PubMedCentralPubMedGoogle Scholar
  183. Yamaguchi Y, Kamiya Y, Nambara E (2007) Regulation of ABA and GA levels during seed development and maturation in Arabidopsis. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell, Scientific Publishers, Oxford, pp 224–247Google Scholar
  184. Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T (2010) Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol 51:2031–2046PubMedGoogle Scholar
  185. 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 16:367–37PubMedCentralPubMedGoogle Scholar
  186. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35:155–189Google Scholar
  187. Yoshioka T, Endo T, Satoh S (1998) Restoration of seed germination at supraoptimal temperatures by fluridone, an inhibitor of abscisic acid biosynthesis. Plant Cell Physiol 39:307–312Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Seed Biotechnology Center, Department of Plant SciencesUniversity of CaliforniaDavisUSA

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