Nitrogen compounds stress indicators in response to toxic doses of Nitrogen and deficient in green beans
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Phaseolus vulgaris L.
osmoprotectores Phaseolus vulgaris L.

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Sánchez Chávez, E., Ruiz, J. M., & Romero, L. (2016). Nitrogen compounds stress indicators in response to toxic doses of Nitrogen and deficient in green beans. Nova Scientia, 8(16), 228–245.


Introduction: A wide range of environmental factors, such as lower temperature, drought, alkalinity, salinity, nutrient deficiency and toxicity stresses are potentially harmful to plants.
The role of nitrogen as an essential nutrient and structural component of amino acids, proteins, nucleic acids and other essential components for the development has been widely documented in several species because of the importance in the processes of growth and agricultural production. However, at present, there is little literature the effect of nitrogen deficiency and toxicity on osmoregulators compounds as indicators of stress in plants. So the aim of this work was to study nitrogen compounds indicators of stress (proline, glycine betaine and choline) in response to toxic doses of N and deficient in green beans developed in a culture chamber under controlled conditions.

Method: The nitrogen was applied to the nutrient solution in the form of NH4NO3 and increasing doses: N1 = 1.5 mM, N2 = 3.0 mM, N3 = 6.0 mM, N4 = 12.0 mM, N5 = 18.0 mM and N6 = 24.0 mM of N. The parameters analyzed were biomass accumulation, the concentration of proline, glycine betaine and choline in leaves, roots, seeds and pods of green beans cv. Strike.

Results: The application of deficient and toxic doses of N affected the production of biomass in beans, toxic doses being the most affecting this parameter. Furthermore, note that the osmoregulators proline, glycine betaine and choline accumulated only under conditions of N toxicity (N6), however, under conditions of stress caused by a lack of N (N1) accumulation of these compounds does not occur.

Discussion and Conclusion: The stress indicators nitrogen compounds accumulate only low toxicity conditions N (N6), however under conditions of stress caused by deficiency of N accumulation of these compounds does not occur so that could be defined as only the stress bioindicators toxicity of N. Finally, the accumulation of proline, glycine betaine and choline could act as a source of N in the cell under stress, where the accumulation of these nitrogen compounds could be used as a way of storing N.
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Ahmad R, Lim C, Kwon SY. (2013). Glycine betaine: A versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses. Plant Biotechnology Reports 7: 49-57.

Ashraf M, Foolad M. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59(2): 206-216.

Benton Jones JJr. (1997). The essential elements. In: Hydroponics: A practical guide for the soilles grower. Benton Jones J Jr (ed.) St. Lucie Press, Boca Raton, Florida, pp: 30-32.

Blasco B, Rios JJ, Cervilla LM, Sánchez-Rodríguez E, Ruiz JM, Romero L. (2008). Iodine biofortification and antioxidant capacity of lettuce patential benefits for cultivation and human health. Annals of Applied Biology 152: 289-299.

Brill J, Hoffmann T, Bleisteiner M, Bremer E. (2011). Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity. Journal of Bacteriology 193(19): 5335-5346.

Britto DT, Kronzucker HJ. (2013). Ecological significance and complexity of N-source preference in plants. Annals of Botany 112(6): 957-963.

Chen TH, Murata N. (2011). Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant, cell & environment 34(1): 1-20.

Ciompi S, Gentili E, Guidi L, Soldatini GF. (1996). The effect of nitrogen deficiency on leaf gas Exchange and chlorophyll fluorescence parameters in sunflower. Plant Science. 118: 177-184.

Colla G, Rouphael Y, Mirabelli C, Cardarelli M. (2011). Nitrogen‐use efficiency traits of mini‐watermelon in response to grafting and nitrogen‐fertilization doses. Journal of Plant Nutrition and Soil Science 174(6), 933-941.

Dandekar AM, Uratsu SL. (1988). A simple base pair change in proline biosynthesis genes causes osmotic stress tolerance. Journal of Bacteriology 170: 5943-5945.

Delauney AJ, Hu CAA, Kavi Kishor PB, Verma DPS. (1993). Cloning of ornithine-δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. Journal of Biological Chemistry 268: 18673-18678.

Delauney AJ, Verma DPS. (1993). Proline biosynthesis and osmo-regulation in plants. The Plant Journal. 4: 215-223.

Evers D, Lefevre I, Legay S, Lamoureux D, Hausman, JF, Rosales RO, Marca LR, Hoffmann L, Bonierbale M, Schafleitner R. (2010). Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. Journal of Experimental Botany 61: 2327-2343.

Fozouni M, Abbaspour N, Doulati Baneh H. (2012). Leaf water potential, photosynthetic pigments and compatible solutes alterations in four grape cultivars under salinity. Vitis 51(4): 147-152.

Gonzalez-Dugo V, Durand JL, Gastal F. (2010). Water deficit and nitrogen nutrition of crops. A review. Agronomy for sustainable development 30(3): 529-544.

Grive CM, Gratton R. (1983). Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant and Soil 70: 303-307.

Haghighi M, Kafi M, Fang P. (2012). Photosynthetic activity and N metabolism of lettuce as affected by humic acid. International Journal of Vegetable Science 18(2): 182-189.

Hare PD, Cress WA, Van Staden J. (1999). Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. Journal of Experimental Botany 50: 413-434.

Irigoyen JJ, Emerich EW, Sánchez-Díaz M. (1992). Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia. Plantarum. 84: 55-60.

Jolivet Y, Larher F, Hamelin J. (1982). Osmoregulation in halophytic higher plants: the protective effect of glycine betaine against the heat destabilization of membranes. Plant Science Letter. 25: 193-201.

Kalaji H.M, Bosa K, Kościelniak J, Żuk-Gołaszewska K. (2011). Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany 73: 64-72.

Katschnig D, Broekman R, Rozema J. (2013). Salt tolerance in the halophyte Salicornia dolichostachya Moss: growth, morphology and physiology. Environmental and Experimental Botany 92: 32-42.

Kuznestov VV, Shevyakova NI. (1997). Stress responses of tobacco cells to high temperature and salinity. Proline accumulation and phosphorylation of polypeptides. Physiologia Plantarum 100: 320-326.

Lattanzi FA, Schnyder H, Thornton B. (2004). Defoliation effects on carbon and nitrogen substrate import and tissue-bound efflux in leaf growth zones of grasses. Plant, Cell & Environment. 27(3): 347-356.

Lv WT, Lin B, Zhang M, Hua XJ. (2011). Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiology 156(4): 1921-1933.

Moran JF, Becana M, Iturbide-Ormaetxe I, Frechillas S, Klucas RV, Aparicio-Tejo P. (2002). Drought induces oxidative stress in pea plants. Planta 194: 346-352.

Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD. (1998). The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant Journal 16: 487-496.

Papageorgiou GC, Morata N. (1995). The usually strong stabilizing effects of glycine betaine on the structure and function in the oxygen evolving photosystem-II complex. Photosynthesis Research 44: 243-252.

Rathinasabapathi B, Sigua C, Ho J, Gage DA. (2000). Osmoprotectant β‐alanine betaine synthesis in the Plumbaginaceae: S‐adenosyl‐l‐methionine dependent N‐methylation of β‐alanine to its betaine is via N‐methyl and N, N‐dimethyl β‐alanines. Physiologia Plantarum 109(3): 225-231.

Rhodes D, Handa S, Bressan RA. (1986). Metabolic changes associated with adaptation of plant cells. In: Biochemical and Physiological Mechanisms Associated with Environmental stress tolerance. Cherry JH (ed.), Berlin: Springer-Verlag, pp: 41-62.

Rivero RM, Mestre TC, Mittler RON, Rubio F, García Sánchez F, Martínez V. (2014). The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant, Cell & Environment 37(5): 1059-1073.

Sairam RK, Tyagi A. (2004). Physiology and molecular biology of salinity stress tolerance in plants. Current Science-Bangalore 86(3): 407-421.

Sánchez E, Rivero RM, Ruiz JM, Romero L. (2004). Changes in biomass, enzymatic activity and protein concentration in roots and leaves of green bean plants (Phaseolus vulgaris L. cv. Strike) under high NH4NO3 application rates. Scientia Horticulturae 99: 237-248.

SAS. (1987). SAS/STAT Guide for Personal Computers. Version 6; Statistical Analysis System Institute, Inc.: Cary NC. P. 1028-1056.

Szarka A, Tomasskovics B, Bánhegyi G. (2012). The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. International Journal of Molecular Sciences, 13(4): 4458-4483.

Van Breusegem F, Vranová E, Dat JF, Inzé D. (2001). The role of active oxygen species in plant signal transduction. Plant Science 161(3): 405-414.

Von Wirén N, Gazzarrini S, Frommer WB. (1997). Regulation of mineral nitrogen uptake in plants. Plant and Soil. 196: 191-199.

Wolf B. (1982). A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Communications in Soil Science & Plant Analysis 13(12): 1035-1059.

Yancey P. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology 208: 2819-2830.

Zaifnejad M, Clark RB, Sullivan CY. (1997). Aluminum and water stress effects on growth and proline of sorghum. Journal of Plant Physiology, 150(3): 338-344.

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