##plugins.themes.bootstrap3.article.main##

S. Venkatesan P. Masilamani P. Janaki T. Eevera S. Sundareswaran P. Rajkumar

Abstract

Nitric oxide (NO) is an important signalling molecule employed by plants to control many physiological aspects. This review summarizes that crosstalk between NO/H2O2/Ca2+ signalling pathways that drive pollen tube for sexual reproduction in flowering plants. NO is produced in seeds by both enzymatic and non-enzymatic sources that control many physiological aspects of seeds. The interplay of NO and Reactive oxygen species are likely important players in hormonal crosstalk controlling seed germination and dormancy. Mechanism of seed germination and dormancy is mainly regulated by plant hormones like Abscisic acid (ABA) and Gibberellic acid (GA). Based on mode of action of NO with reference to triggering the germination of crop seeds under abiotic stress condition it is infer that there is a linkage between NO and plant growth regulator production. NO cross-talk with reactive oxygen species (ROS) during abiotic stress condition, modulate the light and hormone depended developmental process in the early stage of plant development. NO action to enhancing abiotic stress tolerance by improving antioxidant enzymes and protection against oxidative damage in many crops are discussed in detail.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

##plugins.themes.bootstrap3.article.details##

##plugins.themes.bootstrap3.article.details##

Keywords

Nitric oxide, Signalling molecule, Sodium nitroprusside, S-nitroso-N-acetylpenicillamine

References
Albertos, P., Romero-Puertas, M. C., Tatematsu, K., Mateos, I., Sanchez-Vicente, I., Nambara, E. and Lorenzo, O. (2015). S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nature Communications, 6(1): 1-10.
Astier, J. and Lindermayr, C. (2012). Nitric oxide-dependent posttranslational modification in plants: an update. International Journal of Molecular Sciences, 13: 15193–15208. https://doi.org/10.3390/ijms131 115193
Astier, J., Besson-Bard, A., Wawer, I., Parent, C., Rasul, S., Jeandroz, S., Dat, J. and Wendehenne, D. (2010). Nitric oxide signalling in plants: cross-talk with Ca2+, protein kinases and reactive oxygen species. Annual Plant Reviews, 42: 147–170. https://doi.org/10.1002/97811193 12994.apr0454.
Bascon, G., Rubiales, D., Hebelstrup, K.H., Mandon, J., Harren, F.J., Cristescu, S.M., Mur, L.A. and Prats, E., 2017. Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Scientific reports, 7(1): pp.1-15.
Batak, I., Devi, M., Gibal, Z., Grubisic, D., Poff, K. L. and Konjevic, R. (2002). The effects of potassium nitrate and NO-donors on phytochrome A- and phytochrome Bspecific induced germination of Arabidopsis thaliana seeds. Seed Sci. Res. 12: 253–259. https://doi.org/10.1079/SSR2002118.
Beligni, M. V. and Lamattina, L. (1999). Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Biology and Chemistry, 3: 199-208. https://doi.org/10.1006/niox.1999.0222
Beligni, M. V. and Lamattina, L. (1999a). Is nitric oxide toxic or protective? Trends in Plant Science, 4: 299-300. 10.1016/s1360-1385(99)01451-x 
Beligni, M. V. and Lamattina, L. (1999b). Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta, 208: 337-344. 
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. 
Benamar, A., Rolletschek, H., Borisjuk, L., Avelange-Macherel, M. H., Curien, G., Mostefai, H. A., Andriantsitohaina, R. and Macherel, D. (2008). Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim. Biophys. Acta, 1777: 1268–1275. https://doi.org/10.1016/j.bbabio.200 8.0 6.002.
Besson-Bard, A., Astier, J., Rasul, S., Wawer, I., Dubreuil-Maurizi, C., Jeandroz, S. and Wendehenne, D. (2009). Current view of nitric oxideresponsive genes in plants. Plant Science, 177: 302–309.https://doi.org/10.1016/j.plantsci.2009.0 6.006.
Bethke, P. C., Badger, M. R. and Jones. R. L. (2004). Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell, 16: 332–341. DOI: h ttps://doi.or g/10.1105/tpc.01 7822
Bethke, P. C., Libourel, I. G. and Jones, R. L. (2007). Nitric Oxide in Seed Dormancy and Germination, Annu Plant Rev. Vol. 27: Seed Development, Dormancy and Germination. Blackwell Publishing Ltd, 153–175.
Bethke, P. C., Libourel, I. G. L. and Jones, R. L. (2006). Nitric oxide reduces seed dormancy in Arabidopsis. Journal of Experimental Botany, 57: 517-526. https://doi.org/10.1093/jxb/erj060
Bethke, P. C., Libourel, I. G., Aoyama, N., Chung, Y. Y., Still, D. W. and Jones, R. L. (2007). The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol, 143: 1173–1188. https://doi.org /10.1 104/pp.10 6.09 3435
Bright, J., Hiscock, S. J., James, P. E. and Hancock, J. T. (2009). Pollen generates nitric oxide and nitrite: a possible link to pollen-induced allergic responses. Plant Physiology and Biochemistry, 47(1): 49-55. https://doi.org/10.1016/j.plaphy.2008.09.005
Castillo, M. C., Lozano-Juste, J., González-Guzman, M., Rodriguez, L., Rodriguez, P. L. and Leon, J. (2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci. Signal, 8(392): 89. DOI: 10.1126/scisignal.aaa7981
Courtois, C., Besson, A., Dahan, J., Bourque, S., Dobrowolska, G., Pugin, A. and Wendehenne, D. (2008). Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. Journal of Experimental Botany, 59: 155-163. https://doi.org/10.1093/jxb/erm197
Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D. and Breusegem, F. (2000). Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci, 57: 779–795.
Erusalimsky, J. D. and Moncada, S. (2007). Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler. Thromb. Vasc, 27: 2524–2531. https://doi.org/10.1161/ATVBAHA.10 7.151 167
Farooq, M., Basra, S. M. A., Wahid, A. and Rehman, H. (2009). Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). Journal of Agronomy and Crop Science, 195(4): 254-261. https://doi.org/10.1111/j.1439-037X.2009.00367.x
Feijó, J. A. (2010). The mathematics of sexual attraction. Journal of biology, 9(3): 18. http://www.biomedcentral.com/1471-2229/10/32
Ferrari, T. and Varner, J. E. (1969). Substrate induction of nitrate reductase in barley aleurone layers. Plant Physiol, 44: 85–88. DOI: https://doi.org/10.1104/pp.44.1.85
Ferrari, T. E. and Varner, J. E. (1970). Control of nitrate reductase activity in barley aleurone layers. Proc. Natl. Acad. Sci, 65: 729–736. https://doi.org/10.1073/pnas.65.3.729
Ferrer, M. A. and Barcelo, A. (1999). Differential effects of nitric oxide on peroxidase and H2O2 production by the xylem of Zinnia elegans. Plant, Cell and Environment, 22: 891-897.https://doi.org/10.1046/j.1365-3040.1999.00459.x
Filippou, P., Antoniou, C. and Fotopoulos, V. (2013). The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radical Biology and Medicine, 56: 172-183.https://doi.org/10.1016/j.freeradbiomed.2012.09.0 37
Finkelstein, R. R. and Lynch, T. J. (2000). The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant cell, 12: 599–610. DOI: https://doi.org/10.1105/tpc.12.4.599
Freschi, L. (2013). Nitric oxide and phytohormone interactions: current status and perspectives. Frontiers in Plant Science, 4: 398. https://doi.org/10.3389/fpls.2013.00398
Garcia-Mata, C. and Lamattina, L. (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology, 126: 1196-1204.  https://doi.org/10.1104/pp.126.3.1196
Giba, Z., Grubisic, D. and Konjevic, R. (2007). Seeking the role of NO in breaking seed dormancy, in: L. Lamattina, J. Polacco (Eds.), Nitric Oxide in Plant Growth, Development and Stress Physiolog. Springer, 91–111.
Gibbs, D. J., Isa, N. M., Movahedi, M., Lozano-Juste, J., Mendiondo, G. M., Berckhan, S. and Bassel, G. W. (2014). Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Molecular Cell, 53(3): 369-379. https://doi.org/10.1016/j.molcel.2013.12.020
Grubisic, D., Giba, Z. and Konjevic, R. (1992). The effect of organic nitrates in phytochromecontrolled germination of Paulownia tomentosa seeds. Photochem. Photobiol, 56: 629–632.  https://doi.org/10.1 111/j.1751-1097.1992.tb02213.x
Grun, S., Lindermayr, C., Sell, S. and Durner, J. (2006). Nitric oxide and gene regulation in plants. Journal of Experimental Botany, 57: 507–516. https://doi.org/10.1093/jxb/erj053
Gutermuth, T., Lassig, R., Portes, M. T., Maierhofer, T., Romeis, T., Borst, J. W. and Konrad, K. R. (2013). Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. The Plant Cell, 25(11): 4525-4543. DOI: https://doi.org/10.1105/tpc.113.118463
Hayat, S., Yadav, S., Alyemeni, M. N. and Ahmad, A. (2014). Effect of sodium nitroprusside on the germination and antioxidant activities of tomato (Lycopersicon esculentum Mill). Bulg J Agric Sci, 20(1): 140-4.
Hsu, Y. T. and Kao, C. H. (2004). Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regulation, 42: 227-238. 
Huang, C., He, W., Guo, J., Chang, X., Su, P. and Zhang, L. (2005). Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. Journal of Experimental Botany, 56(422): 3041-3049. https://doi.org/10.1093/jxb/eri301
Jovanovic, V., Giba, Z., Djokovic, D., Milosavljevic, S., Grubisic, D. and Konjevic, R. (2005). Gibberellic acid nitrite stimulates germination of two species of light-requiring seeds via the nitric oxide pathway. Ann. N.Y. Acad. Sci, 1048: 476–481. https://doi.org/10.1196/annals.1342.070
Keeley, J. E. and Fotheringham, C. J. (1997). Trace gas emissions and smoke-induced seed germination. Science, 276: 1248–1250. DOI: 10.1126/science.2 76.53 16.1248
Keeley, J. E. and Fotheringham, C. J. (1998). Smoke-induced seed germination in California chaparral. Ecology, 79: 2320–2336. https://doi.org/10.1890/0 012-9658
Khattab, H. (2007). Role of glutathione and polyadenylic acid on the oxidative defense systems of two different cultivars of canola seedlings grown under saline conditions. Aust J Basic Appl Sci, 1(3): 323–334.
Lamattina, L., García-Mata, C., Graziano, M. and Pagnussat, G. (2003). Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology, 54(1): 109-136. https://doi.org/10.1146/annurev.arpl ant.54.031902.134752
Laspina, N. V., Groppa, M. D., Tomaro, M. L. and Benavides, M. P. (2005). Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Science, 169: 323-330. https://doi.org/10.1016 j.plantsci.200 5.02.0 07
Leshem, Y. Y. (1996). Nitric oxide in biological systems. Plant Growth Regulation, 18: 155–159.
Liu, Y., Shi, L., Ye, N., Liu, R., Jia, W. and Zhang, J. (2009). Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytol, 183: 1030–1042. https://doi.org/10.1111/j.1469-8137.2009.02 89 9.x
Lopez-Molina, L., Mongrand, S. and Chua, N. H. (2001). A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad.Sci, 98: 4782–4787.  https://doi.org/10.1 07 3/p nas.0815942 98
Luu, D.T., Marty-Mazars, D., Trick, M., Dumas, C., and Heizmann, P. (1999). Pollen-stigma adhesion in Brassica spp involves SLG and SLR1 glycoproteins. Plant Cell 11: 251–262. DOI: https://doi.org/10.1105/tpc.11.2.251
Mata-Perez, C., Sanchez-Calvo, B., Padilla, M. N., Begara-Morales, J. C., Valderrama, R., Corpas, F. J. and Barroso, J. B. (2017). Nitro-fatty acids in plant signaling: new key mediators of nitric oxide metabolism. Redox Biology, 11: 554–561. https://doi.org/10.1016/j.redox.20 17.01.0 02
Miles, A. M., Wink, D. A., Cook, J. C. and Grisham, M. B. (1996). Determination of nitric oxide using fluorescence spectroscopy. Enzymol, 268: 105–120.
Mur, L. A., Mandon, J and Persijn, S. (2013). Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants, 5: 52. https://doi.or g/10.1093/a obpla/pls052
Neill, S. J., Desikan, R. and Hancock, J. T. (2003). Nitric oxide signalling in plants. New Phytologist, 159: 11-35.  https://doi.org/10.1046/j.1469-8137.20 03.00 804.x
Neill, S. J., Desikan, R., Clarke, A. and Hancock, J. T. (2002). Nitric oxide is a novel component of abscisic acid signalling in stomatal guard cells. Plant Physiology, 128: 13-16.  DOI: https://doi.org/10.110 4/pp.010707
Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., Ribeiro, D. and Wilson, I. (2008). Nitric oxide, stomatal closure, and abiotic stress. J. Exper. Bot, 59: 165–176. https://doi.org/10.1093/jxb/erm293
Okamoto, M., Kuwahara, A., Seo, M., Kushiro, T., Asami, T., Hirai, N., Kamiya, Y., Koshiba, T. and Nambara, E. (2006). CYP707A1 and CYP707A2, which encode abscisic acid 8 -hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol, 141: 97–107. DOI: https://doi.org/10.1104/pp.106.079475
Pagnussat, G. C., Simontacchi, M., Puntarulo, S. and Lamattina, L. (2002). Nitric oxide is required for root organogenesis. Plant Physiology, 129: 954-956. DOI: https://doi.org/10.1104/pp.004036
Palanivelu, R. and Preuss, D. (2006). Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biology, 6(1): 7.
Pandey, S., Kumari, A., Shree, M., Kumar, V., Singh, P., Bharadwaj, C. and Gupta, K. J. (2019). Nitric oxide accelerates germination via the regulation of respiration in chickpea. Journal of experimental botany, 70(17): 4539-4555. https://doi.org/10.1093/jxb/erz185
Pedroso, M. C., Magalhaes J. R. and Durzan, D. (2000). Nitric oxide induces cell death in Taxus cells. Plant Sci, 157: 173-180. https://doi.org/10.1016/S0168-9452(00)00278-8
Ramadan, A. A., Abd Elhamid, E. M. and Sadak, M. S. (2019). Comparative study for the effect of arginine and sodium nitroprusside on sunflower plants grown under salinity stress conditions. Bulletin of the National Research Centre, 43(1): 118.
Romero-Puertas, M. C., Perazzolli, M., Zago, E. D. and Delledonne, M. (2004). Nitric oxide signalling functions in plant–pathogen interactions. Cellu. Microbiol, 6: 795-803. https://doi.org/10.1111/j.1462-5822.2004.00428.x
Signorelli, S. and Considine, M. J. (2018). Corrigendum: Nitric Oxide Enables Germination by a Four-Pronged Attack on ABA-Induced Seed Dormancy. Frontiers in plant science, 9: 654. https://doi.org/10.3389/fpls.2018.00296
Takayama, S., Shiba, H., Iwano, M., Asano, K., Hara, M., Che, F.S., Watanabe, M., Hinata, K., and Isogai, A. (2000). Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc. Natl. Acad. Sci. USA 97: 3765–3770. https://doi.org/10.1073/pnas.9 7.7.3 765
Tawfik, M. M., Badr, E. A., Ibrahim, O. M., Abd Elhamid, E. M. and Sadak, M. S. (2017). Biomass and some physiological aspects of Spartina patens grown under salt affected environment in South Sinai. inter. J Agric Res, 12(1): 17-26. https://scialert.net/abstract/?doi=ijar.2017.1 9.27
Therond, P., Bonnefont-Rousselot, D., Davit-Spraul, A., Conti, M. and Legrand, A. (2000). Biomarkers of oxidative stress: an analytical approach. Current Opinion in Clinical Nutrition and Metabolic Care, 3: 373-384.  
Wang, P., Zhu, J. K. and Lang, Z. (2015). Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant signaling & behavior, 10(6): 103-193. https://doi.org/10.1080/15592324.2015.1031939
Wany A, Gupta KJ. 2018. Reactive oxygen species, nitric oxide production and antioxidant gene expression during development of aerenchyma formation in wheat. Plant Signaling & Behavior, 13: e1428515. https://doi.org/10.1080/15592324.2018.1428515
Wilkins, K. A., Bancroft, J., Bosch, M., Ings, J., Smirnoff, N. and Franklin-Tong, V. E. (2011). Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of papaver. Plant Physiology, 156(1): 404-416. DOI: https://doi.org/10.1104/pp.110.167510
Wilson, I. D., Neill, S. J. and Hancock, J. T. (2008). Nitric oxide synthesis and signalling in plants. Plant Cell Environ, 31: 622–631.
Yamasaki, H. (2000). Nitrite-dependent nitric oxide production pathway: Implications for involvement of active nitrogen species in photoinhibition In vivo. Phil. Trans. R. Soc. Lond. Biol. Sci, 355: 1477-1488. https://doi.org/10.1098/rstb.2000.0708
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.
Zanardo, D. I. L., Zanardo, F. M. L., Ferrarese, M. L. L., Magalhaes, J. R. and Ferrarese-Filho, O. (2005). Nitric oxide affecting seed germination and peroxidase activity in canola (Brassica napus L.). Physiology and Molecular Biology of Plants, 11: 81-86. 
Zhao, L., Zhang, F., Guo, J., Yang, Y., Li, B. and Zhang, L. (2004). Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology, 134: 848-857.  DOI: https://doi.org/10.1104/pp.103.030023
Zhao, M., Zhao, X., Wu, Y. and Zhang, L. (2007). Enhanced sensitivity to oxidative stress in an Arabidopsis nitric oxide synthase mutant. Journal of Plant Physiology, 164: 737-745. https://doi.org/10.1016/j.jplph.2006.03.002
Citation Format
How to Cite
Venkatesan, S., Masilamani , P. ., Janaki, P. ., Eevera, T. ., Sundareswaran, S. ., & Rajkumar, P. . (2020). Role of nitric oxide in seed biology and seed production: A review. Journal of Applied and Natural Science, 12(3), 277-287. https://doi.org/10.31018/jans.v12i3.2290
More Citation Formats:
Section
Research Articles