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Nitrogen oxides as environmental sensors for seeds

Published online by Cambridge University Press:  22 February 2007

Zlatko Giba ,
Dragoljub Grubišić  and
Radomir Konjević
Zlatko Giba
Affiliation:
Institute of Botany, Faculty of Biology, University of Belgrade, Yugoslavia
Dragoljub Grubišić
Affiliation:
Institute for Biological Research ‘Siniša Stankovic’, 29 novembra 142, Belgrade 11060, Yugoslavia
Radomir Konjević*
Affiliation:
Institute of Botany, Faculty of Biology, University of Belgrade, Yugoslavia
*
*Correspondence: Fax: +381 11769903 Email: [email protected]
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Abstract

Nitrates have long been known to promote seed germination in many species, and various proposals have been made regarding the role of nitrates in this process. One hypothesis suggests a possible ecological role for nitrate, providing the seeds with a report of soil nitrogen status and the proximity of already established plants. However, nitrogen oxides (NO, NO2), which are present in the soil, also may be information carriers that indicate not only soil nitrate content, but also microbial activity and, therefore, soil quality. Because of annual variation of soil trace gas fluxes, seeds could be provided with information on seasonal and climate changes in their surroundings. Thus, nitrogen oxides would be the outer information carriers providing the seeds with integral data about many important factors required for successful germination and seedling establishment.

Keywords

seed ecologynitrogen oxidesgerminationsmokesoil trace gases
Type
Research Article
Information
Seed Science Research , Volume 13 , Issue 3 , September 2003 , pp. 187 - 196
Copyright
Copyright © Cambridge University Press 2003

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References

Adkins, S.W., Simpson, G.M. and Naylor, J.M. (1984) The physiological basis of seed dormancy in Avena fatua. IV. Alternative respiration and nitrogenous compounds. Physiologia Plantarum 60, 234–238.CrossRefGoogle Scholar
Appenroth, K.J., Augsten, H. and Mohr, H. (1992) Photophysiology of turion germination in Spirodela polyrhiza (L.) Schleiden. X. Role of nitrate in the phytochrome-mediated response. Plant, Cell and Environment 15, 743–748.CrossRefGoogle Scholar
Baldwin, I.T., Staszak-Kozinski, L. and Davidson, R. (1994) Up in smoke. I. Smoke-derived germination cues for post-fire annual Nicotiana attenuata Torr. ex. Watson. Journal of Chemical Ecology 20, 2345–2371.CrossRefGoogle Scholar
Ballard, L.A.T. (1973) Physical barriers to germination. Seed Science and Technology 1, 285–303.Google Scholar
Barnes, J.D. and Wellburn, A.R. (1998) Air pollutant combinations. pp. 147–164in De Kok, L.J.;Stulen, I. (Eds). Responses of plant metabolism to air pollution and global change. Leiden, Backhuys Publishers.Google Scholar
Baskin, J.M. and Baskin, C.C. (1985) The annual dormancy cycle in buried weed seeds: A continuum. BioScience 35, 492–498.CrossRefGoogle Scholar
Batak., I., Devíé, M., Giba, Z., Grubišić, D., Poff, K.L. and Konjević, R. (2002) The effects of potassium nitrate and NO donors on phytochrome A- and phytochrome B-specific induced germination of Arabidopsis thaliana seeds. Seed Science Research 12, 253–259.CrossRefGoogle Scholar
Baxter, B.J.M. and van Staden, J. (1994) Plant-derived smoke: an effective seed pretreatment. Plant Growth Regulation 14, 279–282.CrossRefGoogle Scholar
Bean, P.A. (1962) An enquiry into the effect of veld fires on certain geophytes. MSc thesis, University of Cape Town.Google Scholar
Beckman, J.S., Beckman, T.W., Chen, J., Marshall, P.A. and Freeman, B.A. (1990) Apparent hydroxyl radical production by peroxynitrite: Implication for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences, USA 87, 1620–1624.CrossRefGoogle ScholarPubMed
Beligni, M.V. and 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.CrossRefGoogle ScholarPubMed
Bell, D.T., Plummer, J.A. and Taylor, S.K. (1993) Seed germination ecology in southwestern Western Australia. Botanical Review 59, 24–73.CrossRefGoogle Scholar
Bell, D.T., King, L.A. and Plummer, J.A. (1999) Ecophysiological effects of light quality and nitrate on seed germination in species from Western Australia. Australian Journal of Ecology 24, 2–10.CrossRefGoogle Scholar
Bewley, J.D. and Black, M. (1982) Physiology and biochemistry of seeds in relation to germination. 2. Viability, dormancy and environmental control. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Blackmer, A.M. and Cerrato, M.E. (1986) Soil properties affecting formation of nitric oxide by chemical reactions of nitrite. Soil Science Society of America Journal 50, 1215–1218.CrossRefGoogle Scholar
Bowler, C., Neuhaus, G., Yamagata, H. and Chua, N.H. (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77, 73–81.CrossRefGoogle ScholarPubMed
Brimblecombe, P. and Stedman, D.H. (1982) Historical evidence for a dramatic increase in the nitrate component of acid rain. Nature 298, 460–462.CrossRefGoogle Scholar
Brown, N.A.C. (1993) Promotion of germination of fynbos seeds by plant-derived smoke. New Phytologist 123, 575–584.CrossRefGoogle ScholarPubMed
Brown, N.A.C. (1994) First the gas, now instant dehydrated smoke. Veld and Flora 80, 72–73.Google Scholar
Brown, N.A.C. and van Staden, J. (1997) Smoke as a germination cue: a review. Plant Growth Regulation 22, 115–124.CrossRefGoogle Scholar
Brown, N.A.C., Botha, P.A. and Prosh, D. (1995) Where there's smoke. Garden (London) 120, 402–405.Google Scholar
Burrows, N., Gardiner, G., Ward, B. and Robinson, A. (1990) Regeneration of Eucalyptus wandoo following fire. Australian Forestry 53, 248–258.CrossRefGoogle Scholar
Caro, A. and Puntarulo, S. (1999) Nitric oxide generation by soybean embryonic axes. Possible effect on mitochondrial function. Free Radical Research 31, S205–S212.CrossRefGoogle ScholarPubMed
Cattanio, J.H., Davidson, E.A., Nepstad, D.C., Verchot, L.V. and Ackerman, I.L. (2002) Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia. Biology and Fertility of Soils 36, 102–108.Google Scholar
Chambers, D.P. and Attiwill, P.M. (1994) The ash-bed effect in Eucalyptus regnans forest: chemical, physical, and microbiological changes in soil after heating or partial sterilization. Australian Journal of Botany 42, 739–749.CrossRefGoogle Scholar
Christianson, C.B. and Cho, C.M. (1983) Chemical denitrification of nitrite in frozen soils. Soil Science Society of America Journal 7, 38–42.CrossRefGoogle Scholar
Cohn, M.A. (1987) Mechanisms of physiological seed dormancy. pp. 14–20in Frazier, G.W.; and Evans, R.A., (Eds). Seed and seedbed ecology of rangeland plants. Washington, DC, USDA-ARS.Google Scholar
Cohn, M.A. (1996) Chemical mechanisms of breaking seed dormancy. Seed Science Research 6, 95–99.CrossRefGoogle Scholar
Cohn, M.A. and Castle, L. (1984) Dormancy in red rice. IV. Response of unimbibed and imbibing seeds to nitrogen dioxide. Physiologia Plantarum 60, 552–556.CrossRefGoogle Scholar
Cohn, M.A., Butera, D.L. and Hughes, J.A. (1983) Seed dormancy in red rice. III. Response to nitrite, nitrate and ammonium ions. Plant Physiology 73, 381–384.CrossRefGoogle ScholarPubMed
Conrad, R. (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiological Reviews 60, 609–640.CrossRefGoogle ScholarPubMed
Cooney, R.V., Harwood, P.J., Custer, L.J. and Franke, A.A. (1994) Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environmental Health Perspectives 102, 460–462.CrossRefGoogle ScholarPubMed
Corbineau, F., Bagniol, S. and Come, D. (1990) Sunflower (Helianthus annuus L.) seed dormancy and its regulation by ethylene. Israel Journal of Botany 39, 313–325.Google Scholar
Corpas, F.J., Barosso, J.B. and del Rio, L.A. (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends in Plant Science 6, 145–150.CrossRefGoogle ScholarPubMed
Crutzen, P.J. (1979) The role of NO and NO2 in the chemistry of the troposphere and stratosphere. Annual Review of Earth and Planetary Sciences 7, 443–472.CrossRefGoogle Scholar
Davidson, C.A., Kaminski, P.M., Wu, M.D., and Wolin, M.S. (1996) Nitrogen dioxide causes pulmonary arterial relaxation via thiol nitrosation and NO formation. American Journal of Physiology–Heart and Circulatory Physiology 39, H1038–H1043.CrossRefGoogle Scholar
Davidson, E.A. (1992) Sources of nitric and nitrous oxide following wetting of dry soil. Soil Science Society of America Journal 56, 95–102.CrossRefGoogle Scholar
Dean, J.V. and Harper, J.E. (1988) The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiology 88, 389–395.CrossRefGoogle ScholarPubMed
De Lange, J.H. and Boucher, C. (1990) Autoecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. South African Journal of Botany 56, 700–703.CrossRefGoogle Scholar
Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA 98, 13454–13459.CrossRefGoogle ScholarPubMed
Derkx, M.P.M. and Karssen, C.M. (1994) Are seasonal dormancy patterns in Arabidopsis thaliana regulated by changes in seed sensitivity to light, nitrate and gibberellin. Annals of Botany 73, 129–136.CrossRefGoogle Scholar
Dixon, K.W., Roche, S. and Pate, J.S. (1995) The promotive effect of smoke-derived from burnt native vegetation on seed germination of Western Australian plants. Oecologia 101, 185–192.CrossRefGoogle ScholarPubMed
Doherty, L.C. and Cohn, M.A. (2000) Seed dormancy in red rice. XI. Commercial liquid smoke elicits germination. Seed Science Research 10, 415–421.CrossRefGoogle Scholar
Drewes, F.E., Smith, M.T. and van Staden, J. (1995) The effect of plant-derived smoke extract on the germination of light-sensitive lettuce seed. Plant Growth Regulation 16, 205–209.CrossRefGoogle Scholar
Durner, J., Wendehenne, D. and Klessig, D.F. (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of National Academy of Sciences, USA 95, 10328–10353.CrossRefGoogle ScholarPubMed
Furuya, M. and Schäfer, E. (1996) Photoperception and signalling of induction reactions by different phytochromes. Trends in Plant Sciences 1, 301–307.CrossRefGoogle Scholar
Galbally, I.E. and Roy, C.R. (1978) Loss of fixed nitrogen from soils by nitric oxide exhalation. Nature 275, 734–735.CrossRefGoogle Scholar
Giba, Z. (1992) The effect of white light, growth regulators and temperature on the germination of blueberry (Vaccinium myrtillus. L.) seeds. MSc Thesis, University of Belgrade (in Serbian).Google Scholar
Giba, Z. (1998) Modified phytochrome action in. Paulownia tomentosa. seed germination. PhD Thesis, University of Belgrade.Google Scholar
Giba, Z., Grubišić, D. and Konjević, R. (1992) Sodium nitroprusside – stimulated germination of common chick weed (Stellaria media L.) seeds. Archives of Biological Sciences 44, 17P–18P.Google Scholar
Giba, Z., Grubišić, D. and Konjević, R. (1995) The involvement of phytochrome in light-induced germination of blueberry (Vaccinium myrtillus L.) seeds. Seed Science and Technology 23, 11–19.Google Scholar
Giba, Z., Grubišić, D., Sajc, L., Stojaković, D. and Konjević, R. (1997a) Effect of some nitric oxide donors and methylene blue on light-induced germination of Paulownia tomentosa seeds. Archives of Biological Sciences 49, 15P–16P.Google Scholar
Giba, Z., Skordilis, A., Grubišić, D., Thanos, C.A. and Konjević, R. (1997b) Control of seed germination in Mountain Pine. First Balkan Botanical Congress Abstracts, Thessaloniki, Greece, p. 95.Google Scholar
Giba, Z., Grubišić, D., Todorović, S., Sajc, L., Stojaković, D. and Konjević, R. (1998a) Effect of nitric oxide-releasing compounds on phytochrome-controlled germination of Empress tree seeds. Plant Growth Regulation 26, 175–181.CrossRefGoogle Scholar
Giba, Z., Todorović, S., Grubišić, D. and Konjević, R. (1998b) Occurrence and regulatory roles of superoxide anion radical and nitric oxide in plants. Iugoslavica Physiologica et Pharmacologica Acta 34, 447–461. Available at website http://www.ippa.bg.ac.yu (verified May 2003).Google Scholar
Goel, A., Kumar, G., Payne, G.F. and Dube, S.K. (1997) Plant cell biodegradation of a xenobiotic nitrate ester, nitroglycerin. Nature Biotechnology 15, 174–177.CrossRefGoogle ScholarPubMed
Goudey, J.S., Saini, H.S. and Spencer, M.S. (1988) Role of nitrate in regulating germination of Sinapis arvensis L. (wild mustard). Plant, Cell and Environment 11, 9–12.CrossRefGoogle Scholar
Gouvea, C.M.C.P., Souza, J.F., Magalhaes, A.C.N. and Martins, I.S. (1997) NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regulation 21, 183–187.CrossRefGoogle Scholar
Grubišić, D. and Konjević, R. (1990) Light and nitrate interaction in phytochrome-controlled germination of Paulownia tomentosa seeds. Planta 181, 239–243.CrossRefGoogle Scholar
Grubišić, D., Giba, Z. and Konjević, R. (1991) Organic nitrates stimulated germination of common chick weed (Stellaria media L.) seeds. Arhiv Bioloških Nauka 43, 7P–8P.Google Scholar
Grubišić, D., Giba, Z. and Konjević, R. (1992) The effect of organic nitrates in phytochrome-controlled germination of Paulownia tomentosa seeds. Photochemistry and Photobiology 56, 629–632.CrossRefGoogle Scholar
Grubišić, D., Giba, Z. and Konjević, R. (1995) Seed germination of Gentiana cruciata L. Bulletin de l‘Institut et du Jardin Botaniques de l’ Universite de Beograd 29, 93–100.Google Scholar
Guerinot, M.L. and Yi, Y. (1994) Iron: nutritious, noxious and not readily available. Plant Physiology 104, 815–820.CrossRefGoogle Scholar
Haas, C.J. and Scheuerlein, R. (1991) Nitrate effect on phytochrome-mediated germination in fern spores: Investigation on the mechanism of nitrate action. Journal of Plant Physiology 138, 350–357.CrossRefGoogle Scholar
Hilhorst, H.W.M. and Karssen, C.M. (1989) Nitrate reductase independent stimulation of seed germination of Sisymbrium officinale L. (hedge mustard) by light and nitrate. Annals of Botany 63, 131–137.CrossRefGoogle Scholar
Hilton, J.R. (1985) The influence of light and potassium nitrate on the dormancy and germination of Avena fatua L. (wild oat) seed stored buried and under natural conditions. Journal of Experimental Botany 36, 974–979.CrossRefGoogle Scholar
Hsiao, A.I. and Quick, W.A. (1996) The roles of inorganic nitrogen salts in maintaining phytochrome- and gibberellin A3-mediated germination control in skotodormant lettuce seeds. Journal of Plant Growth Regulation 15, 159–165.CrossRefGoogle Scholar
Huang, X., von Rad, U. and Durner, J. (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215, 914–923.CrossRefGoogle ScholarPubMed
Karssen, C.M. (1982) Seasonal patterns of dormancy in weed seeds. pp. 243–270in Khan, A.A. (Ed.) The physiology and biochemistry of seed development, dormancy and germination. Amsterdam, Elsevier Biomedical Press.Google Scholar
Karssen, C.M. and Hilhorst, H.W.M. (1992) Effect of chemical environment on seed germination. pp. 327–348in Fenner, M. (Ed.) Seeds: The ecology of regeneration in plant communities. Wallingford, CAB International.Google Scholar
Keeley, J.E. (1991) Seed germination and life history syndromes in the California chaparral. Botanical Review 57, 81–116.CrossRefGoogle Scholar
Keeley, J.E. (1993) Smoke-induced flowering in the fire-lily Cyrtanthus ventricosus. South African Journal of Botany, 59, 638CrossRefGoogle Scholar
Keeley, J.E. and Fotheringham, C.J. (1997) Trace gas emissions and smoke-induced seed germination. Science 276, 1248–1250.CrossRefGoogle Scholar
Keeley, J.E. and Fotheringham, C.J. (1998) Smoke-induced seed germination in California chaparral. Ecology 79, 2320–2336.CrossRefGoogle Scholar
Keeley, J.E., Morton, B.A., Pedrosa, A. and Trotter, P. (1985) Role of allelopathy, heat, and charred wood in the germination of chaparral herbs and suffrutescents. Journal of Ecology 73, 445–458.CrossRefGoogle Scholar
Keeley, S.C. and Pizzorno, M. (1986) Charred wood stimulated germination of two fire-following herbs of the California chaparral and the role of hemicellulose. American Journal of Botany 73, 1289–1297.Google Scholar
Kozlov, A.V., Staniek, K. and Nohl, H. (1999) Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Letters 454, 127–130.CrossRefGoogle ScholarPubMed
Larcher, W. (1995) Plants under stress. pp. 340–348. in Physiological plant ecology – Ecophysiology and stress physiology of functional groups. (3rd edition). Berlin, Springer-Verlag.Google Scholar
Lehmann, E. (1909) Zur Keimungphysiologie und -biologie von Ranunculus sclereatus L. und einigen anderen Samen. Berichte der Deutschen Botanischen Gesellschaft 27, 476–494.Google Scholar
Leshem, Y.Y. (1996) Nitric oxide in biological systems. Plant Growth Regulation 18, 155–159.CrossRefGoogle Scholar
Leshem, Y.Y., Wills, R.B.H. and Ku, V.V. (1998) Evidence for the function of the free radical gas – nitric oxide (NO) – as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiology and Biochemistry 36, 825–833.CrossRefGoogle Scholar
Millar, A.H. and Day, D.A. (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Letters 398, 155–158.CrossRefGoogle Scholar
Nielsen, T., Pilegaard, K., Egelov, A.H., Granby, K., Hummelshoj, P., Jensen, N.O. and Skov, H. (1996) Atmospheric nitrogen compounds: occurrence, composition and deposition. Science of Total Environment 190, 459–465.CrossRefGoogle Scholar
Nikolaeva, M.G., Rasumova, M.V. and Gladkova, V.N. (1985) in Danilova, F. (Ed.) Reference book of dormant seed germination.(in Russian). Leningrad, Nauka Publishers.Google Scholar
Noritake, T., Kawakita, K. and Doke, N. (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant and Cell Physiology 37, 113–116.CrossRefGoogle Scholar
O'Neill, P. (1985) Environmental chemistry. London, George Allen and Unwin.CrossRefGoogle Scholar
Palmer, R.M.J., Ashton, D.S. and Moncada, A.S. (1988) Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333, 664–666.CrossRefGoogle ScholarPubMed
Parmeter, J.R. and Uhrenholdt, B. (1975) Some effects of pine needle or grass smoke on fungi. Phytopathology 65, 28–31.CrossRefGoogle Scholar
Pfeiffer, S., Janistyn, B., Jessner, G., Pichorner, H. and Ebermann, R. (1994) Gaseous nitric oxide stimulates guanosine-3,5-cyclic monophosphate (cGMP) formation in spruce needles. Phytochemistry 36, 259–262.CrossRefGoogle Scholar
Pierce, S.M., Esler, K. and Cowling, R.M. (1995) Smoke-induced germination of succulents (Mesembryanthemaceae) from fire-prone and fire-free habitats in South Africa. Oecologia 102, 520–522.CrossRefGoogle ScholarPubMed
Polglase, P.J., Attiwill, P.M. and Adams, M.A. (1986) Immobilization of soil nitrogen following wildfire in two eucalypt forests of south-eastern Australia. Acta Oecologica-Oecologia Plantarum 7, 261–271.Google Scholar
Pons, T.L. (1989) Breaking of seed dormancy by nitrate as a gap detection mechanism. Annals of Botany 63, 139–143.CrossRefGoogle Scholar
Powlson, D.S., Saffigna, P.G. and Kragt-Cottaar, M. (1988) Denitrification at sub-optimal temperatures in soils from different climatic zones. Soil Biology and Biochemistry 20, 719–723.CrossRefGoogle Scholar
Remde, A., Slemr, F. and Conrad, R. (1989) Microbial production and uptake of nitric oxide in soil. FEMS Microbiology Ecology 62, 221–230.CrossRefGoogle Scholar
Reyes, O. and Casal, M. (1998) Germination of Pinus pinaster, P. radiata and Eucalyptus globulus in relation to amount of ash produced in forest fires. Annales des Sciences Forestières 55, 837–845.CrossRefGoogle Scholar
Roberts, E.H. (1973) Oxidative processes and the control of seed germination. pp. 189–231in Heydecker, W. (Ed.) Seed ecology. London, Butterworths.Google Scholar
Ruge, U. (1955) Zur Analyse der Saatguterhitzung von Malvaceen. Beiträge zur Biologie der Pflanzen 31, 409–417.Google Scholar
Schneider, M., Luxenhofer, O., Deissler, A. and Ballschmiter, K. (1998) C1-C15 alkyl nitrates, benzyl nitrate, and bifunctional nitrates: Measurement in California and South Atlantic air and global comparison using C2Cl4 and CHBr3 as marker molecules. Environmental Science and Technology 32, 3055–3062.CrossRefGoogle Scholar
Shinomura, T., Nagatani, A., Chory, J. and Furuya, M. (1994) The induction of seed germination in Arabidopsis thaliana is regulated principally by phytochrome B and secondarily by phytochrome A. Plant Physiology 104, 363–371.CrossRefGoogle ScholarPubMed
Shinomura, T., Nagatani, A., Hanzawa, H., Kubota, M., Watanabe, M. and Furuya, M. (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 8129–8133.CrossRefGoogle ScholarPubMed
Skiba, U., Hargreaves, K.J., Fowler, D. and Smith, K.A. (1992) Fluxes of nitric and nitrous oxides from agricultural soils in a cool temperate climate. Atmospheric Environment, Part A –. General Topics, 26, 2477–2488.CrossRefGoogle Scholar
Slemr, F. and Seiler, W. (1991) Field study of environmental variables controlling the NO emissions from soil and the NO compensation point. Journal of Geophysical Research 96, 13017–13031.CrossRefGoogle Scholar
Stöhr, C., Strube, F., Marx, G., Ulrich, W.R. and Rockel, P. (2001) A plasma-membrane bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212, 835–841.Google ScholarPubMed
Stushnoff, C. and Hough, L.F. (1968) Response of blueberry seed germination to temperature, light, potassium nitrate and coumarin. Proceedings of the American Society for Horticultural Science 93, 260–266.Google Scholar
Taylor, J.L.S. and van Staden, J. (1996) Root initiation in Vigna radiata (L.) Wilczek hypocotyl cuttings is stimulated by smoke-derived extracts. Plant Growth Regulation 18, 165–168.CrossRefGoogle Scholar
Thanos, C.A. and Rundel, P.W. (1995) Fire-followers in chaparral: nitrogenous compounds trigger seed germination. Journal of Ecology 83, 207–216.CrossRefGoogle Scholar
Thanos, C.A. and Skordilis, A. (1987) The effects of light, temperature and osmotic stress on the germination of Pinus halepensis and P. brutia seeds. Seed Science and Technology 15, 163–174.Google Scholar
Thanos, C.A., Georghiou, K., Kadis, C. and Pantazi, C. (1992) Cistaceae: a plant family with hard seeds. Israel Journal of Botany 41, 251–263.Google Scholar
Thomas, P.A. and Wein, R.W. (1994) Amelioration of woody ash toxicity and jack pine establishment. Canadian Journal of Forest Research 24, 748–755.CrossRefGoogle Scholar
Thomas, T.H. and van Staden, J. (1995) Dormancy break of celery (Apium graveolens L.) seeds by plant-derived smoke extract. Plant Growth Regulation 17, 195–198.CrossRefGoogle Scholar
Thornton, F.C. and Valente, R.J. (1996) Soil emissions of nitric oxide and nitrous oxide from no-till corn. Soil Science Society of America Journal 60, 1127–1133.CrossRefGoogle Scholar
Toole, E.H., Toole, V.K., Borthwick, H.A. and Hendricks, S.B. (1955) Photocontrol of Lepidium seed germination. Plant Physiology 30, 15–21.CrossRefGoogle ScholarPubMed
Torreilles, J. (2001) Nitric oxide: one of the more conserved and widespread signaling molecules. Frontiers in Bioscience 6, D1161–D1172.Google ScholarPubMed
Tortoso, A.C. and Hutchinson, G.L. (1990) Contributions of autotrophic and heterotrophic nitrifiers to soil NO and N2O emissions. Applied and Environmental Microbiology 56, 1799–1805.CrossRefGoogle Scholar
van Cleemput, O. and Samater, A.H. (1996) Nitrite in soils: accumulation and role in the formation of gaseous N compounds. Fertilizer Research 45, 81–89.CrossRefGoogle Scholar
van Staden, J., Drewes, F.E. and Jäger, A.K. (1995) The search for germination stimulants in plant-derived smoke extracts. South African Journal of Botany 61, 260–263.CrossRefGoogle Scholar
van Staden, J., Jäger, A.K. and Strydom, A. (1995) Interaction between plant-derived smoke extract, light and phytohormones on the germination of light-sensitive lettuce seeds. Plant Growth Regulation 17, 213–218.CrossRefGoogle Scholar
Vujičić, R., Grubišić, D. and Konjević, R. (1993) Scanning electron microscopy of the seed coat in the genus Paulownia (Scrophulariaceae). Botanical Journal of the Linnean Society 111, 505–511.CrossRefGoogle Scholar
Walter, H. (1983) Vegetation of the earth and ecological systems of the geo-biosphere. Berlin, Springer-Verlag.Google Scholar
Wendehenne, D., Pugin, A., Klessig, D.F. and Durner, J. (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends in Plants Science 6, 177–183.CrossRefGoogle ScholarPubMed
Wentworth, P., Wentworth, A.D., Zhu, X., Wilson, I.A., Janda, K.D., Eschenmoser, A. and Lerner, R.A. (2003) Evidence for the production of trioxygen species during antibody-catalyzed chemical modification of antigens. Proceedings of the National Academy of Sciences, USA 100, 1490–1493.CrossRefGoogle ScholarPubMed
Wicklow, D.T. (1977) Germination response on Emmenanthe penduliflora (Hydrophylaceae). Ecology 58, 201–205.CrossRefGoogle Scholar
Yamasaki, H., Sakihama, Y. and Takahashi, S. (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends in Plant Science 4, 128–129.CrossRefGoogle ScholarPubMed
Yamulki, S., Harrison, R.M., Goulding, K.W.T. and Webster, C.P. (1997) N2O, NO and NO2 fluxes from a grassland: effect of soil pH. Soil Biology and Biochemistry 29, 1199–1208.CrossRefGoogle Scholar
Ye, R.W., Averill, B.A. and Tiedje, J.M. (1994) Denitrification: production and consumption of nitric oxide. Applied and Environmental Microbiology 60, 1053–1058.CrossRefGoogle ScholarPubMed
Zweier, J.L., Wang, P.H., Samouilov, A. and Kuppusamy, P. (1995) Enzyme-independent formation of nitric oxide in biological tissues. Nature Medicine 1, 804–809.CrossRefGoogle ScholarPubMed