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Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production

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Abstract

Mature seeds of apple (Mallus domestica Borb. cv. Antonówka) are dormant and do not germinate unless their dormancy is removed by several weeks of moist-cold treatment. We investigated the effect of short-term (3 h) nitric oxide (NO) pretreatment on breaking of apple embryonic dormancy expressed as inhibition of germination and morphological abnormalities of young seedlings. Imbibition of embryos isolated from dormant apple seeds with sodium nitroprusside (SNP) or S-nitroso,N-acetyl penicillamine (SNAP) as NO donors resulted in enhanced germination. Moreover, NO treatment removed morphological abnormalities of seedlings developing from dormant embryo. The NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-teramethylimidazoline-1-oxyl-3 oxide (cPTIO) removed the above effects. NO-mediated breaking of embryonic dormancy correlated well with enhanced ethylene production. Inhibitor of ethylene synthesis (AOA) reversed the stimulatory effect of NO donors on embryo germination. Additionally SNP reduced embryo sensitivity to exogenously applied ABA ensuing dormancy breakage. We can conclude that NO acts as a regulatory factor included in the control of apple embryonic dormancy breakage by stimulation of ethylene biosynthesis.

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Abbreviations

ABA:

Abscisic acid

ACC:

1-aminocyclopropane-1-carboxylic acid

AOA:

Aminooxyacetic acid

cPTIO:

2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3 oxide

GA:

Gibberellic acid

SNP:

Sodium nitroprusside

NO:

Nitric oxide

SNAP:

S-nitroso,N-acetyl penicillamine

References

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interaction between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyls elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219:847–855

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Libourel IGL, Jones RL (2006) Nitric oxide reduces seed dormancy in Arabidopsis. J Exp Bot 57:517–526

    Article  PubMed  CAS  Google Scholar 

  • Biddle E, Kerfoot DGS, Kho YH, Russell KE (1976) Kinetic studies of the thermal decomposition of 2-chloroethyphosphonic acid in aqueous solution. Plant Physiol 58:700–702

    Article  PubMed  CAS  Google Scholar 

  • Bogatek R (1995) The possible role of fructose 2,6-bisphosphate in the cyanide-mediated removal of embryonic dormancy in apple. Physiol Plant 94:460–464

    Article  CAS  Google Scholar 

  • Bogatek R, Sykała A (2005) Signaling action of cyanide on ethylene biosynthesis in dormant apple embryos. Eighth international workshop on seeds “germinating new ideas”, Brisbane, Australia, pp 72

  • Bogatek R, Dziewanowska K, Lewak St (1991) Hydrogen cyanide and embryonal dormancy in apple seeds. Physiol Plant 83:417–421

    Article  CAS  Google Scholar 

  • Bogatek R, Come D, Corbineau F, Ranjan R, Lewak St (2002) Jasmonic acid affects dormancy and sugar catabolism in germinating apple embryos. Plant Physiol Biochem 40:167–173

    Article  CAS  Google Scholar 

  • Bogatek R, Gawrońska H, Oracz K (2003) Involvement of oxidative stress and ABA in CN-mediated elimination of embryonic dormancy in apple. In: Nicolas G, Bradford KJ, Come D, Pritchard HW (eds) The biology of seeds: recent research advances. CABI Publishing, Wallingford, pp 211–216

    Google Scholar 

  • Calvo AP, Nicolas C, Lorenzo O, Nocolas G, Rodriguez D (2004) 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 23:44–53

    Article  CAS  Google Scholar 

  • Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588

    Article  PubMed  CAS  Google Scholar 

  • Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391

    Article  PubMed  CAS  Google Scholar 

  • Ghaseemian 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 12:1117–1126

    Article  Google Scholar 

  • Giba Z, Grubisic D, Todorovic S, Sajc L, Stojakovic D, Konjevic R (1998) Effect of nitric oxide-releasing compounds on phytochrome-controlled germination of empress tree seeds. Plant Growth Regul 26:175–181

    Article  CAS  Google Scholar 

  • Giba Z, Grubisic D, Konjevic R (2003) Nitrogen oxides as environmental sensors for seed. Seed Sci Res 13:187–196

    Article  Google Scholar 

  • Hung KT, Kao CH (2003) Nitric oxide counteracts the senescence of rice leaves induced by abscisic acid. J Plant Physiol 160:871–879

    Article  PubMed  CAS  Google Scholar 

  • Kępczyński J, Kępczyńska E (1997) Ethylene in seed dormancy and germination. Physiol Plant 101:720–726

    Article  Google Scholar 

  • Koornneef M, Bentisink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:1–4

    Article  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulate seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  PubMed  CAS  Google Scholar 

  • Leshem YY, Wills RBH, Veng-Va Ku V (1998) Evidence for the function of the radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833

    Article  CAS  Google Scholar 

  • Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vogeli-Lange R, Meins F Jr (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 38:785–795

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Murgia I, de Pinto MC, Delledonne M, Soave C, de Gara L (2004) Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death and cell redox state in plant cells. J Plant Physiol 161:777–783

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed  CAS  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  PubMed  CAS  Google Scholar 

  • 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 211:144–149

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro DM, Barros RS (2004) Germination of dormant seed of Stylosanthes humilis as promoted by ethylene accumulation in closed environments. Braz J Plant Physiol 16:83–88

    Article  CAS  Google Scholar 

  • del Rio LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    Article  PubMed  CAS  Google Scholar 

  • Scherer GFE (2000) NO donors mimic and NO inhibitors inhibit cytokinin action in betaine accumulation in Amaranthus caudatus. Plant Growth Regul 32:345–350

    Article  CAS  Google Scholar 

  • Seregelyes C, Barna B, Hennig J, Konopka D, Pasternak TP, Lukacs N, Feher A, Horvath GV, Dudits D (2003) Phytoglobins can interfere with nitric oxide functions during plant growth and pathogenic responses: a transgenic approach. Plant Sci 165:541–550

    Article  CAS  Google Scholar 

  • Simontacchi M, Jasid S, Puntarulo S (2004) Nitric oxide generation during early germination of sorghum seeds. Plant Sci 167:839–847

    Article  CAS  Google Scholar 

  • Smoleńska G, Lewak St (1971) Gibberellins and the photosensitivity of isolated embryos from non-stratified apple seeds. Planta 99:144–153

    Article  Google Scholar 

  • Yamasaki H (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ 28:78–84

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors are greatly thankful to K. Tomala and T. Krupa (Department of Pomology, Warsaw Agricultural University, Warsaw, Poland) for help in detection of ethylene emission, and A. Sykała for skilful technical assistance.

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Authors and Affiliations

  1. Department of Plant Physiology, Warsaw Agricultural University, Nowoursynowska 159, 02-776, Warsaw, Poland

    Agnieszka Gniazdowska, Urszula Dobrzyńska, Tomasz Babańczyk & Renata Bogatek

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  1. Agnieszka Gniazdowska
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  2. Urszula Dobrzyńska
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  3. Tomasz Babańczyk
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  4. Renata Bogatek
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Correspondence to Renata Bogatek.

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Gniazdowska, A., Dobrzyńska, U., Babańczyk, T. et al. Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta 225, 1051–1057 (2007). https://doi.org/10.1007/s00425-006-0384-z

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  • DOI: https://doi.org/10.1007/s00425-006-0384-z

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