BACKGROUND AND AIMS: Nitric oxide (NO) is involved in the signalling and regulation of plant growth and development and responses to biotic and abiotic stresses. The photoperiod-sensitive mutant 7B-1 in tomato (Solanum lycopersicum) showing abscisic acid (ABA) overproduction and blue light (BL)-specific tolerance to osmotic stress represents a valuable model to study the interaction between light, hormones and stress signalling. The role of NO as a regulator of seed germination and ABA-dependent responses to osmotic stress was explored in wild-type and 7B-1 tomato under white light (WL) and BL. METHODS: Germination data were obtained from the incubation of seeds on germinating media of different composition. Histochemical analysis of NO production in germinating seeds was performed by fluorescence microscopy using a cell-permeable NO probe, and endogenous ABA was analysed by mass spectrometry. KEY RESULTS: The NO donor S-nitrosoglutathione stimulated seed germination, whereas the NO scavenger 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (PTIO) had an inhibitory effect. Under WL in both genotypes, PTIO strongly suppressed germination stimulated by fluridone, an ABA inhibitor. The stimulatory effect of the NO donor was also observed under osmotic stress for 7B-1 seeds under WL and BL. Seed germination inhibited by osmotic stress was restored by fluridone under WL, but less so under BL, in both genotypes. This effect of fluridone was further modulated by the NO donor and NO scavenger, but only to a minor extent. Fluorescence microscopy using the cell-permeable NO probe DAF-FM DA (4-amino-5-methylamino-2',7'-difluorofluorescein diacetate) revealed a higher level of NO in stressed 7B-1 compared with wild-type seeds. CONCLUSIONS: As well as defective BL signalling, the differential NO-dependent responses of the 7B-1 mutant are probably associated with its high endogenous ABA concentration and related impact on hormonal cross-talk in germinating seeds. These data confirm that light-controlled seed germination and stress responses include NO-dependent signalling.

Department of Biochemistry University Olomouc Czech Republic

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Arasimowicz M, Floryszak-Wieczorek J. Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Science. 2007;172:876–887.

Batak I, Devic M, Giba Z, Grubisic D, Poff K, Konjevic R. The effects of potassium nitrate and NO-donors on phytochrome A and phytochrome B-specific induced germination of Arabidopsis thaliana seeds. Seed Science Research. 2002;12:253–259.

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

Bergougnoux V, Hlavačkova V, Plotzová R, Novák O, Fellner M. The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. Journal of Experimental Botany. 2009;60:1219–1230. PubMed

Beson-Bard A, Pugin A, Wendehenne D. New insights into nitric oxide signalling in plants. Annual Review of Plant Biology. 2008;59:21–39. PubMed

Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. 2004a;16:332–341. PubMed PMC

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

Bethke PC, Libourel IGL, Reinöhl V, Jones RL. Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta. 2006;223:805–812. PubMed

Corpas FJ, Leterrier M, Valderrama R, et al. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Science. 2011;181:604–611. PubMed

Delledonne M. NO news is good news for plants. Current Opinion in Plant Biology. 2005;8:390–396. PubMed

Fellner M, Sawhney VK. Seed germination in a tomato male-sterile mutant is resistant to osmotic, salt and low-temperature stresses. Theoretical and Applied Genetics. 2001;102:215–221.

Fellner M, Sawhney VK. The 7B-1 mutant in tomato shows blue-light-specific resistance to osmotic stress and abscisic acid. Planta. 2002;214:675–682. PubMed

Fellner M, Zhang R, Pharis RP, Sawhney VK. Reduced de-etiolation of hypocotyl growth in a tomato mutant is associated with hypersensitivity to, and high endogenous levels of, abscisic acid. Journal of Experimental Botany. 2001;357:725–738. PubMed

Fellner M, Franklin JA, Reid DM, Sawhney VK. Increased sensitivity to, and reduced production of, ethylene in an ABA-overproducing tomato mutant. Acta Biologica Cracoviensia. 2005;47:205–212.

Garcia-Mata C, Lamattina L. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology. 2001;126:1196–1204. PubMed PMC

Giba Z, Grubisic D, Todorovic S, Sajc L, Stojakovic D, Konjevic T. Effect of nitric oxide-releasing compounds on phytochrome-controlled germination of Empress tree seeds. Plant Growth Regulation. 1998;26:175–181.

Gniazdowska A, Dobrzyńska U, Babańczyk T, Bugatek R. Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta. 2006;225:1051–1057. PubMed

Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell and Environment. 2003;26:1851–1862.

Gubler F, Millar AA, Jacobsen JV. Dormancy release, ABA and pre-harvest sprouting. Current Opinion in Plant Biology. 2005;8:1–5. PubMed

Hradecká V, Novák O, Havlíček L, Strnad M. Immunoaffinity chromatography of abscisic acid combined with electrospray liquid chromatography-mass spectrometry. Journal of Chromatography B. 2007;847:162–173. PubMed

Jiao Y, Yang H, Ma L, et al. A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiology. 2003;133:1480–1493. PubMed PMC

Jiao Y, Lau OS, Deng XW. Light-regulated transcriptional networks in higher plants. Nature Reviews. 2007;8:217–230. PubMed

Jovanovich V, Giba Z, Djokovic D, Milosavljevic S, Grubisic D, Konjevic R. Gibberellic acid nitrite stimulates germination of two species of light-requiring seeds via the nitric oxide pathway. Annals of New York Academy of Science. 2005;1048:476–481. PubMed

Kopyra M, Gwóźdź EA. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiology and Biochemistry. 2003;41:1011–1017.

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

Libourel IGL, Bethke PC, De Michele R, Jones RL. Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: use of a flow-through apparatus for delivery of nitric oxide. Planta. 2006;223:813–820. PubMed

Liu HY, Yu X, Cui DY, et al. The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Research. 2007;17:638–649. PubMed

Liu Y, Shi L, Ye N, Liu R, Jia W, Zhang J. Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytologist. 2009;183:1030–1042. PubMed

Liu Y, Ye N, Liu R, Chen M, Zhang J. H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany. 2010;61:2979–2990. PubMed PMC

Matakiadis T, Alboresi A, Jikumaru Y, et al. The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology. 2009;149:949–960. PubMed PMC

Mur LAJ, Carver TLW, Prats E. NO way to live; the various roles of nitric oxide in plant–pathogen interactions. Journal of Experimental Botany. 2006;57:489–505. PubMed

Murashige T, Skoog A. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum. 1962;15:473–497.

Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I. Nitric oxide evolution and perception. Journal of Experimental Botany. 2008;59:25–35. PubMed

Okamoto M, Kuwahara A, Seo M, et al. CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiology. 2006;141:97–107. PubMed PMC

Planchet E, Kaiser WM. Nitric oxide production in plants – facts and fictions. Plant Signaling & Behavior. 2006;1:46–51. PubMed PMC

Sarath G, Bethke PC, Jones R, Baird LM, Hou G, Mitchell RB. Nitric oxide accelerates seed germination in warm-season grasses. Planta. 2006;223:1154–1164. PubMed

Sarath G, Hou G, Baird LM, Mitchell RB. Reactive oxygen species, ABA and nitric oxide interactions on the germination of warm-season C4-grasses. Planta. 2007;226:697–708. PubMed

Sawhney VK. Genic male sterility. In: Shivanna KR, Sawhney VK, editors. Pollen biotechnology for crop production and improvement. Cambridge, UK: Cambridge University Press; 1997. pp. 183–198.

Sawhney VK. Photoperiod-sensitive male-sterile mutant in tomato and its potential use in hybrid seed production. Journal of Horticultural Science and Biotechnology. 2004;79:138–141.

Shi S, Wang G, Wang Y, Zhang L, Zhang L. Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide. 2005;13:1–9. PubMed

Šírová J, Sedlářová M, Piterková J, Luhová L, Petřivalský M. The role of nitric oxide in the germination of plant seeds and pollen. Plant Science. 2011;181:560–572. PubMed

Turečková V, Novák O, Strnad M. Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Talanta. 2009;80:390–399. PubMed

Valderrama R, Corpas FJ, Carreras A, et al. Nitrosative stress in plants. FEBS Letters. 2007;581:453–461. PubMed

Wilson ID, Neill SJ, Hancock JT. Nitric oxide synthesis and signalling in plants. Plant, Cell and Environment. 2008;31:622–631. PubMed

Zago E, Morsa S, Dat JF, et al. Nitric oxide- and hydrogen peroxide responsive gene regulation during cell death induction in tobacco. Plant Physiology. 2006;141:404–411. PubMed PMC

Zhang X, Takemiya A, Kinoshita T, Shimazaki K. Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signalling pathways in Vicia guard cells. Plant and Cell Physiology. 2007;48:715–23. PubMed

Tomato Root Growth Inhibition by Salinity and Cadmium Is Mediated By S-Nitrosative Modifications of ROS Metabolic Enzymes Controlled by S-Nitrosoglutathione Reductase

Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants