Planta

, Volume 231, Issue 3, pp 653–664 | Cite as

Genes involved in ethylene and gibberellins metabolism are required for endosperm-limited germination of Sisymbrium officinale L. seeds

Germination in Sisymbrium officinale L. seeds
Original Article

Abstract

The rupture of the seed coat and that of the endosperm were found to be two sequential events in the germination of Sisymbrium officinale L. seeds, and radicle protrusion did not occur exactly in the micropylar area but in the neighboring zone. The germination patterns were similar both in the presence of gibberellins (GA4+7) and in presence of ethrel. The analysis of genes involved in GAs synthesis and breakdown demonstrated that (1) SoGA2ox6 expression peaked just prior to radicle protrusion (20–22 h), while SoGA3ox2 and SoGA20ox2 expression was high at early imbibition (6 h) diminishing sharply thereafter; (2) the accumulation of SoGA20ox2 transcript was strongly inhibited by paclobutrazol (PB) as well as by inhibitors of ET synthesis and signaling (IESS) early after imbibition (6 h), while SoGA3ox2 and SoGA2ox6 expression was slowly depressed as germination progressed; (3) ethrel and GA4+7 positively or negatively affected expression of SoGA3ox2, SoGA20ox2, and SoGA2ox6, depending on the germination period studied. Regarding genes involved in ET synthesis, our results showed that SoACS7 was expressed, just prior to radicle emergence while SoACO2 expression slowly increased as germination progressed. Both genes were strongly inhibited by PB but were almost unaffected by externally added ethrel or GA4+7. These results suggest that GAs are more important than ET during the early stages of imbibition, while ET is more important at the late phases of germination of S. officinale L. seeds.

Keywords

ACC- and GAs-oxidases Endospermic seed Ethylene Germination Gibberellins (GA4+7Hedge mustard Mucilage Real-time PCR Sisymbrium 

Abbreviations

ACC

1-Aminocyclopropane-1-carboxylic acid

ABA

Abscisic acid

ET

Ethylene

GAs

Gibberellins

GAox

GA-oxidase

IESS

Inhibitors of ET synthesis and signaling

PB

Paclobutrazol

Supplementary material

425_2009_1073_MOESM1_ESM.doc (130 kb)
Supplementary material 1 (DOC 130 kb)

References

  1. Berridge MV, Tan AS, McCoy KD, Wang R (1996) The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts. Biochemistry 4:15–20Google Scholar
  2. Bethke PC, Libourel IGL, Aoyama N, Chung YY, 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 143:1173–1188PubMedCrossRefGoogle Scholar
  3. Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066PubMedCrossRefGoogle Scholar
  4. Brady SM, McCourt P (2003) Hormone cross-talk in seed dormancy. J Plant Growth Regul 22:25–31CrossRefGoogle Scholar
  5. Calvo AP, Nicolás C, Lorenzo O, Nicolás G, Rodríguez D (2004a) Evidence for positive regulation by gibberellins and ethylene of ACC oxidase expression and activity during transition from dormancy to germination in Fagus sylvatica L. seeds. J Plant Growth Regul 23:44–53CrossRefGoogle Scholar
  6. Calvo AP, Nicolás C, Nicolás G, Rodríguez D (2004b) Evidence for positive cross-talk regulation of a GA20-oxidase (FsGA20ox1) by gibberellins and ethylene during breaking of dormancy in Fagus silvatica seeds. Physiol Plant 120:623–630PubMedCrossRefGoogle Scholar
  7. 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 53:214–224PubMedCrossRefGoogle Scholar
  8. Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode A (2005) The etr1-2 mutation in Arabidopsis thaliana affects the ABA, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48PubMedCrossRefGoogle Scholar
  9. 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 220:251–261PubMedCrossRefGoogle Scholar
  10. De Grauwe L, Vriezen W, Bertrand S, Phillips A, Vidal A, Hedden P, van der Straeten D (2007) Interactions between gibberellin and ethylene signalling pathways in Arabidopsis thaliana. Planta 226:485–498PubMedCrossRefGoogle Scholar
  11. De Grauwe L, Chaerle L, Dugardeyn J, Decat J, Rieu I, Vriezen WH, Moritz T, Beemster GTS, Phillips AL, Harberd NP, Hedden P, van der Straeten D (2008) Reduced gibberellin response affects ethylene biosíntesis and responsiveness in the Arabidopsis gai eto 2-1 double mutant. New Phytol 177:128–141PubMedCrossRefGoogle Scholar
  12. De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarrays analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J 39:537–559PubMedCrossRefGoogle Scholar
  13. Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis? J Exp Bot 59:1–16PubMedCrossRefGoogle Scholar
  14. Fagoaga C, Tadeo FR, Iglesias DJ, Huerta L, Lliso I, Vidal AM, Talón M, Navarro L, García-Martínez JL, Peña L (2007) Engineering of gibberellin levels in citrus by sense and antisense overexpression of a GA20-oxidase gene modifies plant architecture. J Exp Bot 58:1407–1420PubMedCrossRefGoogle Scholar
  15. Feurtado JA, Kermode AR (2007) A merging of paths: abscisic acid and hormonal cross-talk in the control of seed dormancy maintenance and alleviation. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Annu Plant Rev 27:176–223Google Scholar
  16. Finch-Savage WE, Leubner-Metzger L (2006) Seed dormancy and the control of germination. New Phytol 171:501–523PubMedCrossRefGoogle Scholar
  17. Finch-Savage WE, Cadman CS, Toorop PE, Lynn JR, Hilhorst HW (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directly by environment specific sensing. Plant J 51:60–78PubMedCrossRefGoogle Scholar
  18. Gallardo M, Delgado MM, Sánchez-Calle IM, Matilla AJ (1991) Ethylene production and 1-aminocyclopropane-1-carboxylic acid conjugation in thermoinhibited Cicer arietinum L. seeds. Plant Physiol 97:122–127PubMedCrossRefGoogle Scholar
  19. Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2002) Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiol Plant 116:238–247PubMedCrossRefGoogle Scholar
  20. Gong X, Bassel G, Wang A, Greewood JS, Bewley JD (2005) The emergence of embryos from hard seeds is related to the structure of the cell walls of the micropylar endosperm, and not to endo-β-mannanase activity. Ann Bot 96:1165–1173PubMedCrossRefGoogle Scholar
  21. Hilhorst HWM (1990) Dose–response analysis of factors involved in germination and secondary dormancy of seeds of Sisymbrium officinale. Plant Physiol 94:1096–1102PubMedCrossRefGoogle Scholar
  22. Hilhorst HWM, Karssen CM (1988) Dual effect of light on the gibberellins- and nitrate-stimulated seed germination of Sisymbrium officinale and Arabidopsis thaliana. Plant Physiol 86:591–597PubMedCrossRefGoogle Scholar
  23. Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54PubMedCrossRefGoogle Scholar
  24. Hua J, Meyerowitz EM (1998) Ethylene responses and negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271PubMedCrossRefGoogle Scholar
  25. Iglesias-Fernández R, Matilla AJ (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellins pathways during the early imbibition of Sisymbrium officinale L. seeds. J Exp Bot 60:1645–1661PubMedCrossRefGoogle Scholar
  26. Iglesias-Fernández R, Matilla AJ, Pulgar I, de la Torre F (2007) Ripe fruits of Sisymbrium officinale L. contain heterogeneous endospermic seeds with different germination rates. Seed Sci Biotech 1:18–24Google Scholar
  27. Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36PubMedCrossRefGoogle Scholar
  28. Kucera B, Cohn MA, Leubner-Metzger L (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307CrossRefGoogle Scholar
  29. Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyls. Cell 85:183–194PubMedCrossRefGoogle Scholar
  30. Leubner-Metzger L (2002) Seed after-ripening over-expression of class I β-1, 3-gluganase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215:659–698CrossRefGoogle Scholar
  31. Leubner-Metzger L, Petruzzelli L, Waldvogel R, Vögeli-Lange R, Meins F Jr (1998) Ethylene-responsive element binding protein (EREBP) expression and transcriptional regulation of class I β-1, 3 glucanase during tobacco seed germination. Plant Mol Biol 38:785–795PubMedCrossRefGoogle Scholar
  32. 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 41:936–944PubMedCrossRefGoogle Scholar
  33. Lizada MCC, Yang SF (1979) A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Ann Biochem 100:140–145CrossRefGoogle Scholar
  34. Matilla AJ, Matilla-Vázquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–97CrossRefGoogle Scholar
  35. 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 47:864–877PubMedCrossRefGoogle Scholar
  36. Nguyen H, Brown RC, Lemmon BE (2000) The specialized chalazal endosperm in Arabidpsis thaliana and Lepidium virginicum (Brassicaceae). Protoplasma 212:99–110CrossRefGoogle Scholar
  37. Nonogaki H, Chen F, Bradford KJ (2007) Mechanisms and genes involved in germination sensu stricto. In: Bradford K, Nonogaki H (eds) Seed development, dormancy and germination. Annu Plant Rev 27:264–304Google Scholar
  38. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604PubMedCrossRefGoogle Scholar
  39. Pen JR, Harberd NP (2002) The role of GA-mediated signalling in the control of seed germination. Curr Opin Plant Biol 5:376–381CrossRefGoogle Scholar
  40. Penfield S, Meissner RC, Shoue DA, Carpita NC, Bevan MW (2001) MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. Plant Cell 13:2777–2791PubMedCrossRefGoogle Scholar
  41. 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 211:144–149PubMedCrossRefGoogle Scholar
  42. Petruzzelli L, Müller K, Hermann K, Leubner-Metzger G (2003) Distinct expression patterns of β-1, 3-glucanases and chitinases during the germination of solanaceous seed. Seed Sci Res 13:139–153CrossRefGoogle Scholar
  43. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acid Res 29:2002–2007CrossRefGoogle Scholar
  44. Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, López-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20:2729–2745PubMedCrossRefGoogle Scholar
  45. Razem FA, Baron K, Hill RD (2006) Turning on gibberellin and ABA signalling. Curr Opin Plant Biol 9:454–459PubMedCrossRefGoogle Scholar
  46. Rodríguez-Gacio MC, Matilla AJ (2009) Seed dormancy and ABA signalling: the breakthrough goes on. Plant Signal Behav 4:1035–1048CrossRefGoogle Scholar
  47. Saibo NJM, Vriezen WH, Beemster G, Van Der Straeten D (2003) Growth and stomatal development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 33:989–1000PubMedCrossRefGoogle Scholar
  48. Siriwitayawan G, Geneve RL, Downie AB (2003) Seed germination of ethylene perception mutants of tomato and Arabidopsis. Seed Sci Res 13:303–314CrossRefGoogle Scholar
  49. Steel RG, Torrie JH (1982) Principles and procedures of statistics. Mc Graw-Hill, TokyoGoogle Scholar
  50. Toorop PE, van Aelst AC, Hilhorst HWM (2000) The second step of the biphasic endosperm cap weakening that mediates tomato (Lycopersicom esculentum) seed germination is under control of ABA. J Exp Bot 51:1371–1379PubMedCrossRefGoogle Scholar
  51. Vandenbussche F, Vancompernolle B, Rieu I, Ahmad M, Phillips A, Hedden P, Moritz T, Van Der Straeten D (2007) Ethylene-induced Arabidopsis hypocotyl elongation is dependent on but not mediated by gibberellins. J Exp Bot 58:4269–4281PubMedCrossRefGoogle Scholar
  52. Vandendussche F, Vriezen WH, Van Der Straeten D (2006) Ethylene biosynthesis and signaling: a puzzle yet to be completed. In: Hedden P, Thomas SG (eds) Plant hormone signaling. Blackwell, UK, pp 125–145Google Scholar
  53. Verwoerd TC, Dekker BMM, Koekema A (1989) A small-scale procedure for the rapid isolation of RNAs. Nucl Acids Res 17:2362–2368PubMedCrossRefGoogle Scholar
  54. Vriezen WH, Achard P, Harberd NP, Van Der Straeten D (2004) Ethylene mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellic dependent. Plant J 37:505–516PubMedCrossRefGoogle Scholar
  55. Weis D, Ori N (2007) Mechanism of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246CrossRefGoogle Scholar
  56. Western TL, Skinner DJ, Haughn GW (2000) Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol 122:345–355PubMedCrossRefGoogle Scholar
  57. Western TL, Diana S, Young DS, Dean GH, Tan WL, Samuels AL, Haughn GW (2004) MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat. Plant Physiol 134:296–306PubMedCrossRefGoogle Scholar
  58. Yamaguchi S, Kamiya Y, Nambara E (2007) Regulation of ABA and GA levels during seed development and germination in Arabidopsis. In: Bradford K, Nonogaki H (eds) Seed development, dormancy and germination. Annu Plant Rev 27:224–247Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Plant Physiology, Faculty of PharmacyUniversity of Santiago de CompostelaSantiago de CompostelaSpain

Personalised recommendations