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Nitric oxide accelerates seed germination in warm-season grasses

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Abstract

The nitric oxide (NO) donor sodium nitroprusside (SNP) significantly promoted germination of switchgrass (Panicum virgatum L. cv Kanlow) in the light and in the dark at 25°C, across a broad range of concentrations. SNP also promoted seed germination in two other warm-season grasses. A chemical scavenger of NO inhibited germination and blocked SNP stimulation of seed germination. The phenolic (+)-catechin acted synergistically with SNP and nitrite in promoting seed germination. Acidified nitrite, an alternate NO donor also significantly stimulated seed germination. Interestingly, sodium cyanide, potassium ferricyanide and potassium ferrocyanide at 200 μM strongly enhanced seed germination as well, whereas potassium chloride was without effect. Ferrocyanide and cyanide stimulation of seed germination was blocked by an NO scavenger. Incubation of seeds with a fluorescent NO-specific probe provided evidence for NO production in germinating switchgrass seeds. Abscisic acid (ABA) at 10 μM depressed germination, inhibited root elongation and essentially abolished coleoptile emergence. SNP partially overcame ABA effects on radicle emergence but did not overcome the effects of ABA on coleoptile elongation. Light microscopy indicated extension of the radicle and coleoptiles in seeds maintained on water or on SNP after 2 days. In contrast, there was minimal growth of the radicle and coleoptile in ABA-treated seeds even after 3–4 days. These data indicate that seed germination of warm-season grasses is significantly influenced by NO signaling pathways and document that NO could be an endogenous trigger for release from dormancy in these species.

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Abbreviations

ABA :

Abscisic acid

DAF-FM :

4-amino-5-methylamino-2’,7’ difluorofluorescein

NO :

Nitric oxide

PTIO :

2-Phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide

SNP :

Sodium nitroprusside

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Badger MR, Jones RL (2004a) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–41

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bethke PC, Libourel I, Reinhol V, Jones RL (2005) Sodium nitroprusside, cyanide, nitrate and nitrite break Arabidopsis seed dormancy in a nitric oxide dependent manner. Planta, epub ahead of print

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

    Article  PubMed  CAS  Google Scholar 

  • Carlsson S, Wiklund NP, Engstrand L, Weitzburg E, Lundberg JO (2001) Effects of pH, nitrite, and ascorbic acid on nonezymatic nitric oxide generation and bacterial growth in urine. Nitric Oxide 5:580–586

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas AC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Rio LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733

    Article  PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    Article  PubMed  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 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J Exp Bot 395:205–212

    Google Scholar 

  • Goldstein S, Russo A, Samuni A (2003) Reactions of PTIO and carboxy-PTIO with *NO, *NO2, and O2-*. J Biol Chem 278:50949–50955

    Article  PubMed  CAS  Google Scholar 

  • Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol 8:1–5

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hung KT, Kao CH (2005) Hydrogen peroxide is required for abscisic acid induced NH +4 accumulation in rice leaves. J Plant Physiol 162:1022–1029

    PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Seregelyes C, Manac’h N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102

    Article  PubMed  CAS  Google Scholar 

  • Kojima H, Urano Y, Kikuchi K, Higuchi T, Hirata Y, Nagano T (1999) Fluorescent indicators for imaging nitric oxide production. Agnew Chem Int Ed Engl 38:3209–3212

    Article  CAS  Google Scholar 

  • Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36

    Article  PubMed  CAS  Google Scholar 

  • Kundu S, Trent JT III, Hargrove MS (2003) Plants, humans and hemoglobins. Trends Plant Sci 8:387–393

    Article  PubMed  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 

  • Lamotte O, Coutois C, Barnavon L, Pugin A, Wendehenne D (2005) Nitric oxide in plants: the biosynthesis and cell signaling properties of a fascinating molecule. Planta 221:1–4

    Article  PubMed  CAS  Google Scholar 

  • Libourel IGL, Bethke PC, De Michele R, Jones RL (2005) Gaseous nitric oxide stimulates germination of dormant Arabidopsis seeds. Planta, epub ahead of print

  • Lindemayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis thaliana. Plant Physiol 137:921–930

    Article  CAS  Google Scholar 

  • Loch DS, Adkins SW, Heslehurst MR, Paterson MF, Bellairs SM (2004) Seed formation, development, and germination. In: Moser LE, Burson BL, Sollenberger LE (eds) Warm-season (C4) grasses. Agronomy Society of America, Inc. pp 95–144

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    Article  PubMed  CAS  Google Scholar 

  • Planchet E, Gupta KJ, Sonoda M, Kaiser WM (2005) Nitric oxide (NO) emission form tobacco leaves and cell suspensions: rate limiting factors and the evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743

    Article  PubMed  CAS  Google Scholar 

  • Romagosa I, Prada D, Moralejo MA, Sopena A, Munoz P, Casas AM, Swanston JS, Molina-Cano JL (2001) Dormancy, ABA content and sensitivity of a barley mutant to ABA application during seed development and after ripening. J Exp Bot 52:1499–1506

    Article  PubMed  CAS  Google Scholar 

  • Ruzin SE (1992) Plant microtechnique and microscopy. Oxford University Press, New York

    Google Scholar 

  • Shen ZX, Welbaum GE, Parrish DJ, Wolf DD (1999) After-ripening and aging as influenced by anoxia in switchgrass (Panicum virgatum L.) seeds stored at 60°C. Acta Horticulturae 504:191–197

    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 

  • Smart AJ, Moser LE (1999) Switchgrass seedling development as affected by seed size. Agron J 91:335–338

    Article  Google Scholar 

  • Sokolovski S, Hills A, Gay R, Garcia-Mata C, Lamattina L, Blatt MR (2005) Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J 43:520–529

    Article  PubMed  CAS  Google Scholar 

  • Steel RGD, Torrie JH (1982) Principles and procedures of statistics. McGraw Hill, New York

    Google Scholar 

  • Veasey EA, Karasawa MG, Santos PP, Rosa MS, Mamani E, Oliveira GC (2004) Variation in the loss of seed dormancy during after-ripening of wild and cultivated rice species. Ann Bot (Lond) 94:875–882

    Article  CAS  Google Scholar 

  • Wu J, Xu X, Verstraete W (2001) The bactericidal effect and chemical reactions of acidified nitrite under conditions simulating the stomach. J Appl Microbiol 90:523–529

    Article  Google Scholar 

  • Zarnstorff ME, Keys RD, Chamblee DS (1994) Growth regulator and seed storage effects on switchgrass germination. Agron J 86:667–672

    Article  Google Scholar 

  • Zentella R, Yamauchi D, Ho TH (2002) Molecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. Plant Cell 14:2289–2301

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Cynthia Larsen and Ashley Hejny for technical assistance. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. This work is published as Journal Series No. 14,608 from the Agriculture Research Division, University of Nebraska.

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Correspondence to Gautam Sarath.

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Sarath, G., Bethke, P.C., Jones, R. et al. Nitric oxide accelerates seed germination in warm-season grasses. Planta 223, 1154–1164 (2006). https://doi.org/10.1007/s00425-005-0162-3

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