Influence of Nitrogen on Physiological Responses to Bicarbonate in a Grapevine Rootstock

  • Julio Molina
  • José Ignacio CovarrubiasEmail author
Research Article


The presence of bicarbonate in soils is an important inducer of nutritional deficiencies in some grapevine genotypes. The aim of this experiment was to assess the effects of different nitrogen sources on physiological variables in the grapevine rootstock 110 Richter grown in a sub-alkaline media. Plants of the grapevine rootstock 110 Richter were treated with different nitrogen sources (NO3, NH4+, or NH4NO3) in a nutrient solution enriched with bicarbonate. Root enzyme (PEPC, MDH, CS, NADP+-IDH) activities, organic acid concentrations in roots, plant growth and leaf greenness, leaf gas exchange, and mineral concentrations in leaves were determined. The presence of NH4+ promoted an enhancement in leaf greenness, and the treated plants did not trigger physiological response mechanisms to nutritional deficiencies in the roots. However, NH4+ decreased the leaf K concentration. On the other hand, the presence of NO3 in the nutrient solution decreased the leaf greenness, and increased the organic acid concentration in the roots, indicating that these plants were affected by nutritional deficiencies. Instead, intermediate results were obtained in plants treated with NH4NO3. Under the experimental conditions used in this experiment, treatments did not significantly influence the plant biomass, the activity of some enzymes related to organic acids biosynthesis, and the leaf gas exchange. These results suggest that the presence of NH4+ can be an effective strategy to alleviate the negative effects on plant nutrition induced by bicarbonate in plants, an alternative to the soil acidification through inorganic acid applications to the soil.


Ammonium Nitrate Organic acids Leaf greenness Bicarbonate 



This study has been supported by the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of Chile (project “Desarrollo del Área de Nutrición Vegetal en el Departamento de Producción Agrícola de la Facultad de Ciencias Agronómicas de la Universidad de Chile” - PAI - No 7912010003).


This study was funded by the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of Chile (project “Desarrollo del Área de Nutrición Vegetal en el Departamento de Producción Agrícola de la Facultad de Ciencias Agronómicas de la Universidad de Chile” - PAI - No 7912010003).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43(3):345–353CrossRefGoogle Scholar
  2. Cambrollé J, García JL, Figueroa ME, Cantos M (2014) Physiological responses to soil lime in wild grapevine (Vitis vinifera ssp. sylvestris). Environ Exp Bot 105:25–31CrossRefGoogle Scholar
  3. Chen Y, Wang Y, Yeh K (2017) Role of root exudates in metal acquisition and tolerance. Curr Opin Plant Biol 39:66–72CrossRefGoogle Scholar
  4. Chollet R, Vidal J, O’Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Phys 47:273–298CrossRefGoogle Scholar
  5. Covarrubias JI, Rombolà AD (2013) Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate. Plant Soil 370(1–2):305–315CrossRefGoogle Scholar
  6. Covarrubias JI, Rombolà AD (2015) Organic acids metabolism in roots of grapevine rootstocks under severe iron deficiency. Plant Soil 394(1–2):165–175CrossRefGoogle Scholar
  7. Covarrubias JI, Pisi A, Rombolá AD (2014) Evaluation of sustainable management techniques for preventing iron chlorosis in the grapevine. Aust J Grape Wine Res 20:149–159CrossRefGoogle Scholar
  8. Covarrubias JI, Retamales C, Donnini S, Rombolà AD, Pastenes C (2016) Contrasting physiological responses to iron deficiency in cabernet sauvignon grapevines grafted on two rootstocks. Sci Hortic 199:1–8CrossRefGoogle Scholar
  9. Donnini S, De Nisi P, Gabotti D, Tato L, Zocchi G (2012) Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability. Plant. Cell Environ 35(6):1171–1184CrossRefGoogle Scholar
  10. Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54:585–593CrossRefGoogle Scholar
  11. Granja F, Covarrubias JI (2018) Evaluation of acidifying nitrogen fertilizers in avocado trees with iron deficiency symptoms. J Soil Sci Plant Nutr 18(1):157–172Google Scholar
  12. Jelali N, Wissal M, Dell’orto M, Abdellya C, Gharsallia M, Zocchi G (2010) Changes of metabolic responses to direct and induced Fe deficiency of two Pisum sativum cultivars. Environ Exp Bot 68:238–246CrossRefGoogle Scholar
  13. Jimenez S, Gogorcena Y, Hévin C, Rombolà AD, Ollat N (2007) Nitrogen nutrition influences some biochemical responses to iron deficiency in tolerant and sensitive genotypes of Vitis. Plant Soil 290:343–355CrossRefGoogle Scholar
  14. Keller M, Kummer M, Vasconcelos MC (2001) Soil nitrogen utilisation for growth and gas exchange by grapevines in response to nitrogen supply and rootstock. Aust J Grape Wine Res 7:2–11CrossRefGoogle Scholar
  15. Kosegarten H, Hoffmann B, Mengel K (2001) The paramount influence of nitrate in increasing apopastic pH of young sunflower leaves to induce Fe deficiency chlorosis, and the re-greening effect brought about by acidic foliar sprays. J Plant Nutr Soil Sci 164:155–163CrossRefGoogle Scholar
  16. Kronzucker HJ, Szczerba MW, Britto DT (2003) Cytosolic potassium homeostasis revisited: 42K-tracer analysis reveals setpoint variations in [K+]. Planta 217:540–546CrossRefGoogle Scholar
  17. Liu Z, He T, Cao T, Yang T, Meng J, Chen W (2017) Effects of biochar application on nitrogen leaching, ammonia volatilization and nitrogen use efficiency in two distinct soils. J Soil Sci Plant Nutr 17(2):515–528Google Scholar
  18. López-Millán AF, Morales F, Andaluz S, Gogorcena Y, Abadía A, De Las Rivas J, Abadía J (2000) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol 124:885–897CrossRefGoogle Scholar
  19. Loulakakis KA, Morot-Gaudry JF, Velanis CN, Skopelitis DS, Moschou PN, Hirel B, Roubelakis-Angelakis KA (2009) Advancements in nitrogen metabolism in grapevine. In: Roubelakis-Angelakis KA (ed) Grapevine molecular physiology & biotechnology. Springer, Dordrecht, pp 161–205CrossRefGoogle Scholar
  20. Lucena C, Romera FJ, Rojas CL, García MJ, Alcántara E, Pérez-Vicente R (2007) Bicarbonate blocks the expression of several genes involved in the physiological responses to Fe deficiency of strategy I plants. Funct Plant Biol 34:1002–1009CrossRefGoogle Scholar
  21. M’sehli W, Dell’Orto M, De Nisi P, Donnini S, Abdelly C, Zocchi G, Gharsalli M (2009) Responses of two ecotypes of Medicago ciliaris to direct and bicarbonate-induced iron deficiency conditions. Acta Physiol Plant 31:667–673CrossRefGoogle Scholar
  22. Mengel K, Planker R, Hoffmann B (1994) Relationship between leaf apoplast pH and iron chlorosis of sunflower (Helianthus annuus L.). J Plant Nutr 17:1053–1065CrossRefGoogle Scholar
  23. Morales F, Belkhodja R, Abadía A, Abadía J (2000) Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient, field-grown pear trees (Pyrus communis L.). Photosynth Res 63:9–21CrossRefGoogle Scholar
  24. Murtaza B, Murtaza G, Imran M, Amjad M, Naeem A, Shah GM, Wakeel A (2017) Yield and nitrogen use efficiency of rice-wheat cropping system in gypsum amended saline-sodic soil. J Soil Sci Plant Nutr 17(3):686–701CrossRefGoogle Scholar
  25. Neumann G (2006) Root exudates and organic composition of plant roots. In: Luster J, Finlay R (eds) Handbook of methods used in rhizosphere research. Swiss Federal Research Institute WSL, Birmensdorf, p 536Google Scholar
  26. Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2014) K+ uptake in plant roots. The systems involved, their regulation and parallels in other organisms. J Plant Physiol 171(9):688–695CrossRefGoogle Scholar
  27. Nikolic M, Römheld V, Merkt N (2000) Effect of bicarbonate on uptake and translocation of 59Fe in two grapevine rootstocks differing in their resistance to Fe deficiency chlorosis. Vitis 39(4):145–149Google Scholar
  28. Ollat N, Laborde B, Neveux M, Diakou-Verdin P, Renaud C, Moing A (2003) Organic acid metabolism in roots of various grapevine (Vitis) rootstocks submitted to iron deficiency and bicarbonate nutrition. J Plant Nutr 26(10&11):2165–2176CrossRefGoogle Scholar
  29. Römheld V (2000) The chlorosis paradox: Fe inactivation as a secondary event in chlorotic leaves of grapevine. J Plant Nutr 23(11–12):1629–1643CrossRefGoogle Scholar
  30. Santa-María GE, Danna CH, Czibener C (2000) High-affinity potassium transport in barley roots. Ammonium sensitive and insensitive pathways. Plant Physiol 123:297–306CrossRefGoogle Scholar
  31. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardiand MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136(1):2483–2499CrossRefGoogle Scholar
  32. Szczerba, M.W., Britto, D.T., Ali, S.A., Balkos, K.D., Kronzucker, H.J. 2008. NH4 +-stimulated and-inhibited components of K+ transport in rice (Oryza sativa L.). J Exp Bot 59(12), 3415–3423Google Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  1. 1.Facultad de Ciencias AgronómicasUniversidad de ChileSantiagoChile

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