Effects of water deficit during maturation on amino acids and jujube fruit eating quality

Jacinta Collado-González, Zulma N. Cruz, Sonia Medina, Carmen Mellisho, Pedro Rodríguez, Alejandro Galindo, Isabel Egea, Félix Romojaro, Federico Ferreres, Arturo Torrecillas, Angel Gil-Izquierdo


Pear-jujube yield and fruit characteristics can be clearly modified   by a water deficit imposed during fruit maturation period. One essential (cystine (Cys-cys)) and seven non-essential (4-hydroxyproline (p-Hyp), α-aminoadipic acid (AADA), ornithine (orn), β-aminoisobutyric acid (BAIB), α-amino-n-butyric acid (AABA), cystathionine (Cysta) and homocystine (Hcys-cys)) amino acids were identified for the first time. Fruits from plants exposed to a moderate water deficit during the maturation stage (T1) initiated the ripening phase earlier than control (T0) fruits and showed an improved eating quality. Fruits resulting from severe water deficit (T2) showed changes in their physical characteristics and reached more advanced degree of ripening than T0 and T1 fruits, improving not only most of fruit chemical characteristics that make up the taste but also the nutritional value. The decrease in the asparagine (Asn) content of the fruit as a result of severe water deficit is a positive aspect, which prevents acrylamide formation during heat-processing of the fruit.


deficit irrigation; fruit quality; plant water relations; water deficit; LC-MS/MS.

Full Text:



W. H. Outlaw, S. Q. Zhang, K. A. Riddle, A. K. Womble, L. C. Anderson, W. M. Outlaw, N. N. Outlaw, E. C. Outlaw, A. B. Thistle, The jujube (Ziziphus jujuba Mill.), a multipurpose plant, Econ. Bot., 56, 198–200 (2002).

S. Azam-Ali, E. Bonkoungou, C. Bowe, C. Dekock, A. Godara, J. T. Williams, Fruits for the Future 2: Ber and Other Jujubes, Revised ed., International Centre for Underutilised Crops: Southampton, U.K., 2006, p 289.

J. Collado-González, Z. N. Cruz, P. Rodríguez, A. Galindo, F. G. Díaz-Baños, J. García de la Torre, F. Ferreres, S. Medina, A. Torrecillas, A. Gil-Izquierdo, Effect of water deficit and domestic storage on the procyanidin content, size and aggregation process in pear-jujube (Z. jujuba) fruits, J. Agric. Food Chem., 61, 6187−6197 (2013).

S.-H. Choi, J.-B. Ahn, H.-J. Kim, N.-K. Im, N. Kozukue, C. Levin, M. Friedman, Changes in free amino acid, protein, and flavonoid content in jujube (Ziziphus jujuba) fruit during eight stages of growth and antioxidative and cancer cell inhibitory effects by extracts, J. Agric. Food Chem., 60, 10245-10255 (2012).

Q.-H. Gao, C.-S. Wu, M Wang,. B.-N. Xu, L.-J. Du, Effect of drying of jujubes (Ziziphus jujuba Mill.) on the contents of sugars, organic acids, alpha-tocopherol, beta-carotene, and phenolic compounds, J. Agric. Food Chem., 60, 9642-9648 (2012).

S.-H. Choi, J.-B. Ahn, N. Kozukue, C. E. Levin, M. Friedman, Distribution of Free Amino Acids, Flavonoids, Total Phenolics, and Antioxidative Activities of Jujube (Ziziphus jujuba) Fruits and Seeds Harvested from Plants Grown in Korea, J. Agric. Food Chem., 59, 6594-6604 (2011).

J.-W. Li,; L.-P. Fan, S.-D. Ding, X.-L. Ding, Nutritional composition of five cultivars of chinese jujube, Food Chem., 103, 454-460 (2007).

X. Huang, A. Kojima-Yuasa, T. Norikura, D. Kennedy, T. Hasuma, I. Matsui-Yuasa, Mechanism of the anti-cancer activity of Zizyphus jujuba in HepG2 cells, Am. J. Chinese Med., 35, 517-532 (2007).

H.-J. Heo, Y.-J. Park, Y.-M. Suh, S.-J. Choi, M.-J. Kim, H.-Y. Cho, Y.-J. Chang, B. Hong, H.-K. Kim, E. Kim, C.-J. Kim, B.-G. Kim, D.-H. Shin, Effects of oleamide on choline acetyltransferase and cognitive activities, Biosci. Biotech. Bioch., 67, 1284-1291 (2003).

Z. Zhao, M. Liu, P. Tu, Characterization of water soluble polysaccharides from organs of Chinese Jujube (Ziziphus jujuba Mill. cv. Dongzao), Eur. Food. Res. Technol., 226, 985-989 (2008).

R. T. Mahajan, M. Z. Chopda, Phyto-pharmacology of Ziziphus jujuba Mill - A plant review, Pharmacogn. Rev., 3, 320–329 (2009).

H.-S. Kim, Effects of the Zizyphus jujuba seed extract on the lipid components in hyperlipidemic rats, J. Food Sci. Nutr., 7, 72-77 (2002).

S. Guo, J.-A. Duan, Y.-P. Tang, N.-Y. Yang, D.-W. Qian, S.-L. Su, E.-X. Shang, Characterization of triterpenic acids in fruits of Ziziphus species by HPLC-ELSD-MS, J. Agric. Food Chem., 58, 6285-6289 (2010).

F. Mestdagh, B. De Meulenaer, T. Cucu, C. Van Peteghem, Role of water upon the formation of acrylamide in a potato model system, J. Agric. Food Chem., 54, 9092-9098 (2006).

M. Friedman, C. E. Levin, Review of methods for the reduction of dietary content and toxicity of acrylamide, J. Agric. Food Chem., 56, 6113-6140 (2008).

Z. N. Cruz, P. Rodriguez, A. Galindo, E. Torrecillas, S. Ondoño, C. D. Mellisho, A. Torrecillas, Leaf mechanisms for drought resistance in Zizyphus jujuba trees, Plant Sci., 197, 77-83 (2012).

N. Cui, T. Du, S. Kang, F. Li, J. Zhang, M. Wang, Z. Li, Regulated deficit irrigation improved fruit quality and water use efficiency of pear-jujube trees, Agr. Water Manag., 95, 489-497(2008).

R. G. Allen, L. S. Pereira, D. Raes, M. Smith, Crop evapotranspiration: guidelines for computing crop water requirements in:Irrigation and Drainage, FAO, Italy, Rome, 1998, Paper 56.

K. Shackel, A plant-based approach to deficit irrigation in trees and vines, HortScience, 46, 173-177 (2011).

M. I. Egea, P. Sanchez-Bel, M. C. Martinez-Madrid, F. B. Flores, F. Romojaro, The effect of beta ionization on the antioxidant potential of 'Bulida' apricot and its relationship with quality, Postharvest Biol. Tec., 46, 63-70 (2007).

C. D. Mellisho, I. Egea, A. Galindo, P. Rodríguez, J. Rodríguez, W. Conejero, F. Romojaro, A. Torrecillas, Pomegranate (Punica granatum L.) fruit response to different deficit irrigation conditions, Agr. Water Manag., 114, 30-36 (2012).

M. C. Martínez-Madrid, M. Serrano, F. Riquelme, F. Romojaro, Polyamines, abscisic acid and ethylene production in tomato fruit. Phytochemistry, 43, 323-326 (1996).

I. Egea, F. B. Flores, M. C. Martínez-Madrid, F. Romojaro, P. Sánchez-Bel, 1-Methylcyclopropene affects the antioxidant system of apricots (Prunus armeniaca L. cv. Búlida) during storage at low temperature. J. Sci. Food Agric., 90, 549-555 (2010).

P.Sánchez-Bel, I. Egea, F. Romojaro, M. C. Martínez-Madrid, Sensorial and chemical quality of electron beam irradiated almonds (Prunus amygdalus), LWT - Food Sci. Technol., 41, 442-449 (2008).

C. Salazar, J. M. Armenta, D. F. Cortés, V. Shulaev, Combination of an AccQ•Tag-ultra performance liquid chromatographic method with tandem mass spectrometry for the analysis of amino acids, Methods Mol. Biol., 828, 13-28 (2012).

Y. Nagumo, K. Tanaka, K. Tewari, K. Thiraporn, T. Tsuchida, T. Honma, N. Ohtake, K. Sueyoshi, Y. Takahashi, T. Ohyama, Rapid quantification of cyanamide by ultra-high-pressure liquid chromatography in fertilizer, soil or plant samples, J. Chromatogr. A., 1216, 5614-5618 (2009).

S. A. Cohen, Amino acid analysis using pre-column derivatization with 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate: analysis of hydrolyzed proteins and electroblotted samples, in: Methods in Molecular Biology: Protein Sequencing Protocols, 2nd ed., B. J. Smith (Ed), Humana Press Inc., Totowa, New Jersey, 2003, Vol. 211, pp 143-154.

G. Fiechter, H. K. Mayer, UPLC analysis of free amino acids in wines: Profiling of on-lees aged wines. J. Chromatogr. B., 879, 1361-1366 (2011).

B. A. Boughton, D. L. Callahan, C. Silva, J. Bowne, A. Nahid, T. Rupasinghe, D. L. Tull, M. J. McConville, A. Bacic, U. Roessner, Comprehensive profiling and quantitation of amine group containing metabolites, Anal. Chem., 83, 7523-7530 (2011).

SPSS, Inc., SPSS Professional Statistics, Business Intelligence Division, Chicago., 2002, Vol. 12.

D. C. Elfving, A. E. Hall, M. R. Kaufmann, Interpreting leaf water potential measurements with a model of soil-plant-atmosphere continuum, Physiol. Plant., 27, 161-168 (1972).

A. Sellin, Base water potential of Picea abies as a characteristic of the soil water status, Plant Soil., 184, 273-280 (1996).

Q.-H. Gao, P.-T. Wu, J.-R. Liu, C.-S. Wu, J. W. Parry, M. Wang, , Physico-chemical properties and antioxidant capacity of different jujube (Ziziphus jujuba Mill.) cultivars grown in loess plateau of China, Sci. Hortic.-Amsterdam, 130, 67-72 (2011).

C.-S. Wu, Q.-H. Gao, X.-D. Guo, J.-G. Yu, M. Wang, Effect of ripening stage on physicochemical properties and antioxidant profiles of a promising table fruit ‘pear-jujube’ (Zizyphus jujuba Mill.), Sci. Hortic.-Amsterdam, 148, 177-184 (2012).

A. Salvador, J. Cuquerella, J. M. Martinez Javega, 1-MCP treatment prolongs postharvest life of 'Santa Rosa' plums., J. Food Sci., 68, 1504-1510 (2003).

A. A. Kader, Y. Li, A. Chordas, Post-harvest respiration, ethylene production, and compositional changes of chinese jujube fruits, HortScience 17, 678-679 (1982).

M. F. Abbas, R. A. M. Saggar, Respiration rate, ethylene production and certain chemical-changes during the ripening of jujube fruits, J. Hortic. Sci., 64, 223-225 (1989).

M. F. Abbas, B. S. Fandi, Respiration rate, ethylene production and biochemical changes during fruit development and maturation of jujube (Ziziphus mauritiana Lamk), J. Sci. Food Agric., 82, 1472-1476 (2002).

J. H. Al-Niami, R. A. M. Saggar, M. F. Abbas, The physiology of ripening of jujube fruit (Zizyphus spina-christi (L) Wild), Sci. Hortic.-Amsterdam, 51, 303-308 (1992).

Z. Zhang, S. Tian, Z. Zhu, Y. Xu, G. Qin, Effects of 1-methylcyclopropene(1-MCP) on ripening and resistance of jujube (Zizyphus jujuba cv. Huping) fruit against postharvest disease, LWT – Food Sci. Technol., 45, 13-19 (2012).

Q. Wang, T. Lai, G. Qin, S. Tian, Response of jujube fruits to exogenous oxalic acid treatment based on proteomic analysis, Plant Cell Physiol., 50, 230-242 (2009).

Q.-H. Gao, C.-S. Wu, J.-G. Yu, M. Wang, Y.-J. Ma, C.-L. Li, Textural characteristic, antioxidant activity, sugar, organic acid, and phenolic profiles of 10 promising jujube (Ziziphus jujuba Mill.) Selections, J. Food Sci., 77, C1218-C1225 (2012).

Food and Nutrition Board, Commission on Life Sciences, National Research Council, in: Recommended Dietary Allowances, 10th ed. National Academy Press, Washington, DC, United States, 1989.

C. M. Ajila, U. J. S. Prasada Rao, Mango peel dietary fibre: Composition and associated bound phenolics. J .Funct. Foods, 5, 444-450 (2013).

A. Gribaa, F. Dardelle, A. Lehner, C. Rihouey, C. Burel, A. Ferchichi, A. Driouich, J.-C. Mollet, Effect of water deficit on the cell wall of the date palm (Phoenix dactylifera ‘Deglet nour’, Arecales) fruit during development, Plant, Cell Environ., 36, 1056-1070 (2013).

J. C. Favier, J. Ireland-Ripert ,C. Laussucq,M. Feinberg, Table de composition des fruits exotiques, fruits de cueillette d’Afrique,in: Répertoire général des aliments, INRA et Lavoisier (Tec.Doc.) (Eds); Paris, Francia, 1993; Vol 3.

A. Fadavi, M. Barzegar, M. H. Azizi, M. Bayat, Note. Physicochemical composition of ten pomegranate cultivars (Punica granatum L.) grown in Iran, Food Sci. Technol. Int., 11, 113-119 (2005).

M. M. Hussein, Y. E.-D. Camilia, Mineral constituents of Fenugreek varieties grown under water stress condition, Aust. J. Basic Appl. Sci., 5, 2904-2909 (2011).

O. Demirkol, C. Adams, N. Ercal, Biologically important thiols in various vegetables and fruits. J. Agric. Food Chem., 52, 8151-8154 (2004).

L. Zagorchev, C. Seal, I. Kranner, M. Odjakova, A Central role for thiols in plant tolerance to abiotic stress. Int. J. Mol. Sci., 14, 7405-7432 (2013).

P. J. Lea, R. J. Ireland, Nitrogen metabolism in higher plants, in: Plant amino acids: biochemistry and biotechnology, B. Singh(Ed), Marcel Dekker Inc., New York, 1999, pp. 1-47.

K. Zushi, N. Matsuzoe, Free amino acid contents of tomato fruit grown under water and salinity stresses, Acta Hortic., 724, 91-96 (2006).

D. P. Verma, Osmotic stress tolerance in plants: role of proline and sulfur metabolism, in: Molecular responses to cold, drought, heat and salt stress in higher plants,K. Shinozaki and K. Yagamuchi- Shinozaki (Eds), R. G. Landes Company, Texas, 1999; p 153-168.

A. Torrecillas, A. León, F. Del Amor, M. C. Ruiz-Sánchez, Determination of free proline levels in citrus leaf-disks and its relation to xylem potential, Agrochimica, 28, 371-378 (1984).

Q. Ma, D. W. Turner, D. Levy, W. A. Cowling, Solute accumulation and osmotic adjustment in leaves of Brassica oilseeds in response to soil water deficit, Aust. J. Agric. Res., 55, 939-945 (2004).

DOI: http://dx.doi.org/10.20450/mjcce.2014.375


  • There are currently no refbacks.

Copyright (c) 2016 Jacinta Collado-González, Zulma N. Cruz, Sonia Medina, Carmen Mellisho, Pedro Rodríguez, Alejandro Galindo, Isabel Egea, Félix Romojaro, Federico Ferreres, Arturo Torrecillas, Angel Gil-Izquierdo

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.