, Volume 232, Issue 4, pp 999–1005 | Cite as

The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation

  • Agnieszka GniazdowskaEmail author
  • Urszula Krasuska
  • Karolina Dębska
  • Paulina Andryka
  • Renata Bogatek
Rapid Communication


Deep dormancy of apple (Malus domestica Borkh.) seeds is terminated by a 3-month-long cold stratification. It is expressed by rapid germination of seeds and undisturbed growth of seedlings. However, stimulation of germination of isolated apple embryos is also observed after applying inhibitors of cytochrome c oxidase: nitric oxide (NO) or hydrogen cyanide (HCN) during the first 3–6 h of imbibition of dormant embryos. The aim of this work was to compare the effect of yet another toxic gaseous molecule carbon monoxide (CO) with the effects of HCN and NO on germination of apple embryos and growth and development of young seedlings. We demonstrated that stimulation of germination after short-term pre-treatment with HCN, NO or CO was accompanied by enhanced NO emission from the embryo axes during their elongation. Moreover, similarly high NO production from non-dormant embryos, after cold stratification, was detected. Therefore, we propose that NO may act as signaling molecule in apple embryo dormancy break.


Carbon monoxide Hydrogen cyanide Nitric oxide Seed dormancy Seed germination 



Abscisic acid


Carbon monoxide




Hydrogen cyanide


Nitric oxide


Sodium nitroprusside



Part of this work was supported by Ministry of Science and Higher Education of Poland, Grant No. N N303 0905 34.


  1. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39CrossRefPubMedGoogle Scholar
  2. Bethke PC, Liburel IGL, Reinohl V, Jones RL (2006) Sodium nitroprusside, cyanide, nitrite and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223:805–812CrossRefPubMedGoogle Scholar
  3. Boczkowski J, Poderoso JJ, Motterlini R (2006) CO–metal integration: vital signaling from lethal gas. Trends Biochem Sci 31:614–621CrossRefPubMedGoogle Scholar
  4. Bogatek R, Gniazdowska A (2006) Nitric oxide and HCN reduce deep dormancy of apple seeds. Acta Physiol Plant 28:281–287CrossRefGoogle Scholar
  5. Bogatek R, Dziewanowska K, Lewak St (1991) Hydrogen cyanide and embryonal dormancy in apple seeds. Physiol Plant 83:417–421CrossRefGoogle Scholar
  6. Bogatek R, Cóme D, Corbineau F, Picard M-A, Żarska-Maciejewska B, St Lewak (1999) Sugar metabolism as related to the cyanide-mediated elimination of dormancy in apple embryos. Plant Physiol Biochem 37:577–585Google Scholar
  7. Dekker J, Hargrove M (2002) Weedy adaptation in Setaria spp. V. Effects of gaseous environment on giant foxtail (Setaria farberii) (Poaceae) seed germination. Am J Bot 89:410–416CrossRefGoogle Scholar
  8. Eshasi Y, Komatsu H, Ushizawa R, Sakai Y (1982) Breaking of secondary dormancy in cocklebur seeds by cyanide and azide in combination with C2H4 and O2 and their effects on cytochrome and alternative respiratory pathways. Aust J Plant Physiol 9:97–111CrossRefGoogle Scholar
  9. Giba Z, Grubisic D, Konjevic R (2003) Nitrogen oxides as environmental sensors for seeds. Seed Sci Res 13:187–196CrossRefGoogle Scholar
  10. Gniazdowska A, Dobrzyńska U, Babańczyk T, Bogatek R (2007) Breaking of apple embryo dormancy by nitric oxide involves stimulation of ethylene production. Planta 225:1051–1057CrossRefPubMedGoogle Scholar
  11. Gniazdowska A, Krasuska U, Czajkowska K, Bogatek R (2010) Nitric oxide, hydrogen cyanide and ethylene are required in the control of germination and undisturbed development of young apple seedlings. Plant Growth Regul 61:75–84CrossRefGoogle Scholar
  12. Guo K, Xia K, Yang Z-M (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452CrossRefPubMedGoogle Scholar
  13. Hartsfield CL (2002) Cross talk between carbon monoxide and nitric oxide. Antioxid Redox Signal 4:301–307CrossRefPubMedGoogle Scholar
  14. 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 41:1011–1017CrossRefGoogle Scholar
  15. Liu K, Xu S, Xuan W, Ling T, Cao Z, Huang B, Sun Y, Fang L, Liu Z, Zhao N, Shen W (2007) Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci 172:544–555CrossRefGoogle Scholar
  16. Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as positive regulator of root hair development. Plant Signal Behav 1:18–33Google Scholar
  17. Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants—where do we stand? Physiol Plant 138:372–383CrossRefPubMedGoogle Scholar
  18. Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T (2002) Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 130:1958–1966CrossRefPubMedGoogle Scholar
  19. Neill SJ, Desican R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16CrossRefPubMedGoogle Scholar
  20. Nonogaki H, Chen F, Bradford KJ (2007) Mechanisms and genes involved in germination sensu stricto. In: Bradford KJ, Nonogaki H (eds) Seed development dormancy and germination. Blackwell, Oxford, pp 264–304CrossRefGoogle Scholar
  21. Oracz K, El-Maarouf-Bouteau H, Bogatek R, Corbineau F, Bailly C (2008) Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signaling pathway. J Exp Bot 59:2241–2251CrossRefPubMedGoogle Scholar
  22. Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 32:1241–1248CrossRefGoogle Scholar
  23. Roberts EH (1964) The distribution of oxidation-reduction enzymes and the effects of respiratory inhibitors and oxidizing agents on dormancy in rice seed. Physiol Plant 17:14–29CrossRefGoogle Scholar
  24. Salomonson LP, Barber MJ (1990) Assimilatory nitrate reductase: functional properties and regulation. Annu Rev Plant Physiol Plant Mol 41:225–253CrossRefGoogle Scholar
  25. Shapiro AD (2005) Nitric oxide signaling in plants. Vitam Horm 72:339–398CrossRefPubMedGoogle Scholar
  26. Siegel SM, Renwick G, Rosen LA (1962) Formation of carbon monoxide during seed germination and seedling growth. Science 137:683–684CrossRefPubMedGoogle Scholar
  27. Siegień I, Bogatek R (2006) Cyanide action in plants—from toxic to regulatory. Acta Physiol Plant 28:483–497CrossRefGoogle Scholar
  28. Simontacchi M, Jasid S, Puntarulo S (2004) Nitric oxide generation during early germination of sorghum seeds. Plant Sci 167:839–847CrossRefGoogle Scholar
  29. Song XG, She XP, Zhang B (2008) Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiol Plant 132:514–525CrossRefPubMedGoogle Scholar
  30. Wendehenne D, Pugin A, Klessig DF, Durner J (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177–183CrossRefPubMedGoogle Scholar
  31. Xu S, Sa ZS, Cao ZY, Xuan W, Huang BK, Ling TF, Hu Q-Y, Shen W-B (2006) Carbon monoxide alleviates wheat seed germination inhibition and counteracts lipid peroxidation mediated by salinity. J Int Plant Biol 48:1168–1176CrossRefGoogle Scholar
  32. Xuan W, Huang LQ, Li M, Huang BK, Xu S, Liu H, Gao Y, Shen WB (2007) Induction of root elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants? Plant Growth Regul 52:41–51CrossRefGoogle Scholar
  33. Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893CrossRefPubMedGoogle Scholar
  34. Yip WK, Yang SF (1988) Cyanide metabolism in relation to ethylene production in plant tissues. Plant Physiol 88:473–476CrossRefPubMedGoogle Scholar
  35. Zagrobelny M, Bak S, Rasmussen V, Jorgensen B, Naumann CM, Moller BL (2004) Cyanogenic glucosides and plant–insect interactions. Phytochemistry 65:293–306CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Agnieszka Gniazdowska
    • 1
    Email author
  • Urszula Krasuska
    • 1
  • Karolina Dębska
    • 1
  • Paulina Andryka
    • 1
  • Renata Bogatek
    • 1
  1. 1.Department of Plant PhysiologyWarsaw University of Life Science (SGGW)WarsawPoland

Personalised recommendations