Scientia Horticulturae 205 (2016) 79–83

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Review

Crop responses to nitrogen overfertilization: A review

Francisco Albornoz
Departamento de Ciencias Vegetales, Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Av. Vicuña Mackenna 4860,
Macul, Santiago, Chile

a r t i c l e i n f o a b s t r a c t

Article history: Nitrogen-containing fertilizers are commonly used in modern agriculture, but the application rate in
Received 10 November 2015 most fields exceeds crop demand, with short- and long-term negative consequences. Reduction in the
Received in revised form 19 April 2016 quality of the products, assessed by organoleptic characteristics and compounds related to health, such as
Accepted 20 April 2016
nitrate, are commonly reported. Even yield losses, depending on site-specific conditions, can result from
Available online 27 April 2016
N overfertilization. This literature review summarizes the research of the past 20 years that describes the
response of crops to high rates of N fertilization, with a detailed analysis of the conditions and agricultural
Keywords:
practices that lead to nitrate accumulation in leafy green vegetables.
Fertilizers
Nitrate accumulation © 2016 Elsevier B.V. All rights reserved.
Osmotic stress
Yield

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
2. Yield responses to excess N fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
3. Effects on crop quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
4. Nitrate accumulation in leafy green vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
4.1. Varietal differences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
4.2. Agricultural practices to mitigate NO3 − accumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
5. Final remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82

newly developed crop genotypes (Tilman et al., 2002; Good and

1. Introduction Beatty, 2011). By the end of the XXth century, environmental prob-
lems such as groundwater contamination, release of greenhouse
Nitrogen (N) is an essential nutrient required by crops for gases and eutrophication of aquatic ecosystems were correlated
optimal growth and development. Nitrogen is involved in many with heavy N fertilization of fields (Byrnes, 1990; Smith et al., 1999;
physiological and metabolic processes and is key in the structural Harrison and Webb, 2001; Robertson and Vitousek, 2009), which
conformation of plants because it is a primary constituent of pro- forced the implementation of regulatory policies in Europe and the
teins, enzymes and nucleic acids (Maathuis, 2009). Therefore, as a USA to limit the inputs of fertilizers to agricultural fields (Tilman,
limiting resource in agriculture, N is as important as the availability 1998).
of water (Sinclair and Rufty, 2012). Following continual applications of N-containing fertilizers, N
The development of the modern fertilizer industry, which began either accumulates in soils or is lost by runoff or lixiviation (Ju et al.,
in the late XIXth century with the export of sodium nitrate and 2004; Najera et al., 2015). When the N supply exceeds the demand,
bird guano from Chile and Peru to the Northern Hemisphere several physiological responses occur that result in poor quality of
(Melillo, 2012), supported the demands of a growing population the products, which reduces profits for growers. Organic farmers,
that required high yields. During the 1960’s, the ‘Green Revolution’ and most recently agroecologists, argue that poor quality products
provided further encouragement for growers to use high-inputs and reduced profits support the use of fertilizers that promote bio-
of nitrogen fertilizers to obtain the maximum yields possible with logical cycles within soils to promote N release in synchrony with
the environment (Altieri and Nichols, 2003).
When the rate of N application exceeds the requirements of the
E-mail address: fralbornoz@uc.cl crop, yield reductions can also be observed.

http://dx.doi.org/10.1016/j.scienta.2016.04.026
0304-4238/© 2016 Elsevier B.V. All rights reserved.
80 F. Albornoz / Scientia Horticulturae 205 (2016) 79–83
Fig. 1. Schematic of the primary effects of N overfertilization on yield parameters and produce quality.
Based on the literature review, the responses of crops to N over-
fertilization are summarized in Fig. 1, with a description of the
primary characteristics of quality that are affected. Additionally,
alternatives are reviewed that can be used to reduce the negative
effects of N overfertilization.
2. Yield responses to excess N fertilization
Yield reductions for a variety crops occur at high doses of
N fertilization, particularly for fruit trees and fruity vegetables
(e.g., tomato, cucumber and zucchini) (Weinbaum et al., 1992;
Jackson and Lombard, 1993; Tagliavini et al., 2000; Erel et al., 2008;
Stefanelli et al., 2010).
In sweet cherry with fertigation, yield losses of 6–39% occur
at 168 mg N L−1 compared with 84 mg N L−1 (Nielsen et al., 2007).
Similarly, in a recent study of citrus trees in Florida, the optimum
N fertilization rate for the maximum yield is 260 kg N ha−1 year−1 ,
with a quadratic pattern in yield reductions at higher rates of
fertilization (Alva et al., 2006). In olive trees, the number of inflo-
rescences per branch decreases with each increase in the available
N in the root zone above 3.4 mM, which reduces the fruit set (Erel
et al., 2008).
In Cabello et al. (2009), the optimum N fertilization rate for mel-
ons is 90 kg N ha−1 for a marketable yield of 42.9 Mg ha−1 , which is
reduced by 15% with a N fertilization rate of 390 kg N ha−1 . A similar
effect is observed in cucumbers, and the reduction in marketable
yield is associated with a decrease in activity of the enzyme nitrate
reductase in the leaves and a consequent reduction in the export of
amino acids to the fruits (Ruiz and Romero, 1999).
The yield losses in crops receiving high rates of N fertilization
are primarily because of reduced fruit set, which is caused by the
increase in vegetative growth that occurs with the excessive uptake
of N (Weinbaum et al., 1992). In some species, such as apples and
cherries, flower bud initiation is antagonistic with spur vegetative
growth, and flower buds develop only 2–4 weeks after growth of
the spur has ceased (Koutinas et al., 2010). Generally, however, light
intensity is one of the most important factors affecting flower bud
initiation and development (Wilkie et al., 2008), and with excess
N, flower bud development and fruit set are negatively affected
because the increase in vegetative growth increases shading by
foliage (Weinbaum et al., 1992). Additionally, Fernandez-Escobar
et al. (2008) found that the effective pollination period in olive trees
is reduced because of a decrease in the longevity of the ovules under
high, as well as deficient, N fertilization.
For cereal crops, the yield losses associated with high N inputs
were studied as early as 1950 to describe the field conditions
leading to the symptom of ‘haying-off’ that occurred primarily in
dryland wheat (Van Herwaarden et al., 1998). Crops affected by
this disorder ripen prematurely, which results in pinched grains
with a high protein concentration. This disorder is associated with
high N availability in soils during the initial stages of the crop,
which leads to vigorous vegetative growth. However, during post-
anthesis, the availability of water is not sufficient to support the
evapotranspirative demand, and the crop matures with grains low
in carbohydrates and high in proteins (Van Herwaarden et al.,
1998).
Other authors report yield losses in wheat with rates of N fer-
tilization above 240 kg N ha−1 (Wang et al., 2011), which has been
attributed to an osmotic restriction, particularly with nitrate-N fer-
tilizers (Huett, 1996).
3. Effects on crop quality
The quality of agricultural products is assessed based on char-
acteristics such as color, flavor, taste and appearance; however,
each year more consumers are concerned about the nutritional
quality of fruits and vegetable products (Schreiner et al., 2013).
The consumer conception that fruits and vegetables offer ‘healthy
foods’ is based primarily on the content of secondary plant metabo-
lites, including phenolic compounds, glucosinolates (exclusive to
Brassicaceae), flavonoids and carotenoids (Schreiner et al., 2013),
in addition to the absence of harmful compounds such as nitrate
(Konstantopoulou et al., 2010).
Low inputs of N fertilizers enhance these positive characteris-
tics of quality (Stefanelli et al., 2010); however, with excessive N
fertilization, reductions occur in some of these quality parameters
in different crops. For example, the concentration of anthocyanin
in blueberries cv. ‘Duke’ decreased with an increase in the rate of N
fertilization, an effect that was accompanied by a reduction in fruit
size (Ehret et al., 2014). Similarly, the concentrations of vitamin C
and phenolic compounds decrease in a variety of vegetable prod-
ucts that include spinach, tomato and lettuce (Bourn and Prescot,
2002; Zhao et al., 2006; Rembialkowska, 2007; Wang et al., 2008;
Konstantopoulou et al., 2010; Lairon, 2010). To explain these effects
under an ample N supply, plant metabolism likely shifts toward
more N-containing compounds (proteins) to the detriment of com-
pounds that contain more carbon (Rembialkowska, 2007).
High rates of N application also affect the sugar content in prod-
ucts such as potato and sugar beet (Mengel et al., 2001), tomato
(Parisi et al., 2006), apples and pears (Mattheis and Fellman, 1999),
grapes (Jackson and Lombard, 1993), and carrots (Smolen and Sady,
2009).
The concentrations of mineral elements are also reduced at high
N application rates, and significant reductions occur in the calcium
concentrations of tomatoes, cucumbers, apples and kiwis (Sams,
1999; Wang et al., 2008; Fallahi et al., 2010); these reductions are
important because the postharvest life of the product is limited
because of a reduction in firmness (Nielsen et al., 2009).
High rates of N application also reduce the red coloration in
apples, peaches and nectarines, which is an effect directly related
to a decrease in chlorophyll degradation (Kays, 1999; Wargo et al.,
2003; Nielsen et al., 2009; Wang and Cheng, 2011).
 F. Albornoz / Scientia Horticulturae 205 (2016) 79–83 81

Table 1
Maximum levels of nitrate allowed in fresh vegetables by European Union Regulation (EC) No. 1881/2006, amended in 2011.

Product Specifics Maximum level (mg NO3 − kg−1 f.w.)

Fresh spinach (Spinacea oleracea) 3500

Preserved, deep-frozen or frozen spinach 2000
Fresh lettuce (Lactuca sativa) Winter crop:
Grown under cover 5000
Grown in the open air 4000
Summer crop:
Grown under cover 4000
Grown in the open air 3000
“Iceberg” type lettuce Grown under cover 2500
Grown in the open air 2000
Rucola (Eruca sativa, Diplotaxis sp., Brassica tenuifolia, Sisymbrium tenuifolium) Winter crop 7000
Summer crop 6000
Processed cereal-based foods and baby foods for infants and young children 200

Table 2
Distribution of NO3 − concentrations in different types of lettuce sampled in Europe between 2000 and 2007 (EFSA 2008).

Lettuce Nitrate concentration (mg kg−1 f.w.)

type
5th Percentile Average 95th Percentile

Butterhead 53 2026 4090

Cos 167 1105 2200
Curled 16 1601 3400
Escarole 6 523 1579
Iceberg 210 875 1537
Oak-leaf 8 1534 3285

4. Nitrate accumulation in leafy green vegetables
Leafy green vegetables, such as lettuce, spinach, and rucola,
among others, accumulate NO3 − in the leaves, with values that
reach ∼20,000 mg kg−1 f.w. (EFSA, 2008). Because of the effects of
nitrate on aspects of human health (Santamaria, 2006), the Euro-
pean Union limits the NO3 − content in various foodstuffs (Table 1).
Nitrate assimilation is governed by plant growth because the
proportion of organic N relative to those of other constituents of dry
biomass is fixed by the interaction with the environment (Rivas-
Ubach et al., 2012). Therefore, when the rate of uptake exceeds
that of assimilation, NO3 − accumulates in vacuoles (Anjana Umar
and Iqbal, 2007).
Leafy green vegetables reduce NO3 − almost exclusively in the
leaf mesophyll cells. Moreover, coordination with the uptake mech-
anisms in roots is difficult because NO3 − is largely excluded from
the phloem, which limits the feedback regulation of NO3 − trans-
porters (Burns et al., 2011a). In these species, stored NO3 − is a
substitute for carbohydrates in maintaining turgor pressure in
growing tissues. A series of experiments confirm this role for nitrate
(Blom-Zandstra and Lampe, 1985; Burns et al., 2011a); leaf osmotic
pressure is maintained under low rates of CO2 assimilation by
increasing the concentration of NO3 − in the vacuoles.
A positive correlation between NO3 − and whole-plant water
content is observed in lettuce, spinach and tomato. Cardenas-
Navarro et al. (1999) analyzed their data and an extensive data
set from experiments in the literature, which included studies of
more than 60 lettuce genotypes and spinach and tomato. Based on
their analysis, a significant linear correlation (R2 = 0.89) between
NO3 − and plant water content demonstrates that when NO3 − is
less available, plant water content is reduced.
Light is an important environmental factor that controls the
accumulation of NO3 − . Under low light intensities, the photosyn-
thetic synthesis of carbohydrates is reduced, which promotes NO3 −
accumulation. The synthesis and activity of nitrate reductase (NR)
are also limited under reduced light (Lillo, 1994), and reduced NR
activity in the leaves occurs within minutes of the interruption of
light (Riens and Heldt, 1992; Kaiser and Huber, 1994; Lillo, 1994).
The primary purpose of this deactivation is to avoid the accumu-
lation of nitrite (NO2 − ), which is highly toxic and requires redox
equivalents from the activity of photosystem I to be reduced (Riens
and Heldt, 1992).
A distinctive daily pattern of NO3 − accumulation occurs because
of the dependence of NR activity on light intensity (Carrasco and
Burrage, 1992; Schenk, 2004; Gent, 2012). In mature plants, the
NO3 − uptake rate between light and dark hours is not significantly
different (Albornoz and Lieth, 2015a), and therefore, NO3 − accu-
mulates during the night. With the light of a new day, NO3 − exits
the vacuoles and is replaced by the carbohydrates and organic acids
produced by photosynthesis. The concentration of NO3 − is rapidly
reduced during the first hours of light, when the assimilation rate
is two- to threefold higher than the uptake rate (Anjana Umar and
Iqbal, 2007). The assimilation rate decreases toward the end of the
day, primarily because the expression of the genes encoding for NR
is reduced (Stitt, 1999), and stops completely during the night.
4.1. Varietal differences
The NO3 − accumulation capacity is variable for the different
genotypes of commercialized lettuce. Based on a screening con-
ducted within the European Union (Table 2), the lowest average
NO3 − concentrations are in ‘escarole’ and ‘iceberg’ types of lettuce,
whereas the highest concentrations are in ‘oak-leaf’ and ‘curled’
types of lettuce (EFSA, 2008). Several genotypic traits contribute to
these differences that depend on the variety; for example, traits are
different for the capacity of NO3 − transfer to younger leaves (Burns
et al., 2011b); expression of root nitrate transporters (Harrison
et al., 2004); photosynthetic capacity, affecting biomass synthesis
and/or growth rate (Reinink et al., 1987; Behr and Wiebe, 1992);
and NO3 − assimilation capacity (Harada et al., 2004); these differ-
ences lead to the differences in levels of NO3 − accumulation.
4.2. Agricultural practices to mitigate NO3 − accumulation
Unfortunately, nitrate levels in leaves do not change posthar-
vest; therefore, the accumulation must be controlled during
development of the crop (Konstantopoulou et al., 2010).
82 F. Albornoz / Scientia Horticulturae 205 (2016) 79–83
Fig. 2. Leaf yield and NO3 − accumulation in lettuce plants with different concen-
trations of NO3 − in a soilless system. Plants in all treatments were exposed to
supplemental irradiance for a photoperiod of 12 h. Data from Albornoz and Lieth
(2015b).
The most obvious practice is to reduce N fertilizer applications.
Although low N levels in the rhizosphere limit plant growth, high
rates of N application increase yields only to a certain level, and
then NO3 − accumulates in leaves with no further increase in pro-
ductivity (Stefanelli et al., 2011; Albornoz and Lieth, 2015b) (Fig. 2).
In McCall and Willumsen (1999), the yields of greenhouse but-
terhead lettuce grown in soil are not different at N fertilization
rates between 80 and 125 kg N ha−1 , but the NO3 − concentrations
in leaves increase 51% between the lowest and the highest rates
of fertilization. Several authors report similar results (reviewed
by Anjana Umar and Iqbal, 2007). Moreover, extremely high fer-
tilization rates can be detrimental to yields because of osmotic
limitations in the soil solution (Wang and Li, 2004; Albornoz and
Lieth, 2015b).
The use of irrigation techniques such as fertigation ensures
the supply of nutrients to roots with the advantage that sup-
ply can be synchronized with plant demand (Hebbar et al., 2004)
by splitting the total fertilizer application into several smaller
amounts with each irrigation event. Similar results are achieved
using controlled-release fertilizers, with a consequent reduction in
NO3 − accumulation (Ombodi et al., 2010). Two proposed alterna-
tives have been successfully implemented in aeroponic systems:
Demsar et al. (2004) proposed to dynamically modify the N sup-
ply depending on the light intensity, and Albornoz et al. (2014)
suggested a decrease in the supply of NO3 − during the day.
Nitrate accumulation can also be manipulated by using differ-
ent forms of N fertilizer. For example, ammonium-based fertilizers
(i.e., urea, ammonium-nitrate, and ammonium chloride) signifi-
cantly reduce NO3 − accumulation compared with those that are
nitrate-based. The effect of organic fertilizers is similar because of
the low availability of N and N supplied primarily as NH4 + (Zhao
et al., 2006). Biofertilizers also have positive effects and reduce
NO3 − accumulation (Hanafy et al., 2000).
In soilless production, an effective strategy to reduce the con-
centrations of NO3 − in leaves is to withhold N in the days before
harvest (Van Der Boon and Steenhuizen, 1986; Santamaria et al.,
2001). The replacement of NO3 − with other anions such as chlo-
ride (Cl− ) or sulfate (SO4 2− ) produces similar results (Urrestarazu
et al., 1998).
Modifying the supply of light before harvest effectively reduces
NO3 − concentrations independent of environmental and soil con-
ditions. Different sources of supplementary light have been tested,
with the conclusion that photosynthetically active radiation in
red and blue wavelengths by light-emitting diodes (LED) is more
effective than that of other light sources (Samuoliene et al., 2009;
Cometti et al., 2011; Wanglai et al., 2013).
5. Final remarks
Growers are encouraged to reduce and efficiently apply N fertil-
izers to their fields to reduce negative effects on the environment
and to increase the sustainability of their agroecosystems. As an
additional benefit, growers can market products with high contents
of nutraceutical compounds, including vitamins and anthocyanins,
which are all highly rated by consumers worldwide because of their
health benefits. Current breeding programs should target the devel-
opment of cultivars with high N-use efficiency to ensure growers
that N fertilizer applications can be reduced without a reduction in
yields.
References
Albornoz, F., Lieth, J.H., 2015a. Diurnal macronutrients uptake patterns by lettuce
roots under various light and temperature levels. J. Plant Nutr. 38, 1–16.
Albornoz, F., Lieth, J.H., 2015b. Over fertilization limits lettuce productivity because
of osmotic stress. Chilean J. Agric. Res. 75, 284–290.
Albornoz, F., Lieth, J.H., Gonzalez-Fuentes, J.A., 2014. Effect of different day and
night nutrient solution concentration on growth photosynthesis, and leaf NO3 −
content of aeroponically grown lettuce. Chilean J. Agric. Res. 74, 240–245.
Altieri, M.A., Nichols, C.I., 2003. Soil fertility management and insect pests:
harmonizing soil and plant health in agroecosystems. Soil Tillage Res. 72,
203–211.
Alva, A.K., Paramasivam, S., Obreza, T.A., Schumann, A.W., 2006. Nitrogen best
management practice for citrus trees: I. Fruit yield, quality, and leaf nutritional
status. Sci. Hortic. 107, 233–244.
Anjana Umar, S., Iqbal, M., 2007. Nitrate accumulation in plants, factors affecting
the process, and human health implications. A review. Agron. Sustain. Dev. 27,
45–57.
Behr, U., Wiebe, H.J., 1992. Relation between photosynthesis and nitrate content of
lettuce cultivars. Sci. Hortic. 49, 175–179.
Blom-Zandstra, M., Lampe, J.E.M., 1985. The role of nitrate in the osmoregulation of
lettuce (Lactuca sativa L.) growth at different light intensities. J. Exp. Bot. 36,
1043–1052.
Bourn, D., Prescot, J., 2002. A comparison of the nutritional value, sensory qualities
and food safety of organically and conventionally produced foods. Crit. Rev.
Food Sci. 42, 1–34.
Burns, I.G., Zhang, K., Turner, M.K., Edmondson, R., 2011a. Iso-osmotic regulation of
nitrate accumulation in lettuce. J. Plant Nutr. 34, 283–313.
Burns, I.G., Zhang, K., Turner, M.K., Lynn, J., McClement, S., Hand, P., Pink, D., 2011b.
Genotype and environment effects on nitrate accumulation in a diversity set of
lettuce accessions at commercial maturity: the influence of nitrate uptake and
assimilation, osmotic interactions and shoo weight and development. J. Sci.
Food Agric. 9, 2217–2233.
Byrnes, B.H., 1990. Environmental effects of N fertilizer use—an overview. Fert. Res.
26, 209–215.
Cabello, M.J., Castellanos, M.T., Romojaro, F., Martinez-Madrid, C., Ribas, F., 2009.
Yield and quality of melon grown under different irrigation and nitrogen rates.
Agric. Water Manage. 96, 866–874.
Cardenas-Navarro, R., Adamowicz, S., Robin, P., 1999. Nitrate accumulation in
plants: a role for water. J. Exp. Bot. 50, 613–624.
Carrasco, G.A., Burrage, S.W., 1992. Diurnal fluctuations in nitrate uptake and
nitrate accumulation in lettuce (Lactuca sativa L.). Acta Hortic. 339, 137–148.
Cometti, N.N., Martins, M.Q., Bremenkamp, C.A., Nunes, J.A., 2011. Nitrate
concentration in lettuce leaves depending on photosynthetic photon flux and
nitrate concentration in the nutrient solution. Hortic. Bras. 29, 548–553.
Demsar, J., Osvald, J., Vodnik, D., 2004. The effect of light-dependent application of
nitrate on the growth of aeroponically grown lettuce (Lactuca sativa L,). J. Am.
Soc. Hortic. Sci. 129, 570–575.
EFSA (European Food Safety Authority), 2008. Nitrate in vegetables: Scientific
opinion of the panel on contaminants in the food chain. EFSA J. 689, 1–79.
Ehret, D.L., Frey, B., Forge, T., Helmer, T., Bryla, D.R., Zebarth, B.J., 2014. Effects of
nitrogen rate and application method on early production and fruit quality in
highbush blueberry. Can. J. Plant Sci. 94, 1165–1179.
Erel, R., Dag, A., Ben-Gal, A., Schwartz, A., Yermiyahu, U., 2008. Flowering and fruit
set of olive trees in response to nitrogen, phosphorus, and potassium. J. Am.
Soc. Hortic. Sci. 133, 639–647.
Fallahi, E., Fallahi, B., Nielsen, G.H., Nielsen, D., Peryea, F.J., 2010. Effects of mineral
nutrition on fruit quality and nutritional disorders in apples. Acta Hortic. 868,
49–60.
Fernandez-Escobar, R., Ortiz-Urquiza, A., Prado, M., Rapoport, H.F., 2008. Nitrogen
status influence on olive tree flower quality and ovule longevity. Environ. Exp.
Bot. 64, 113–119.
Gent, M.P.N., 2012. Composition of hydroponic lettuce: effect of time of day, plant
size, and season. J. Sci. Food Agric. 92, 542–550.
 F. Albornoz / Scientia Horticulturae 205 (2016) 79–83
Good, A.G., Beatty, P.H., 2011. Fertilizing nature: a tragedy of excess in the
commons. PLoS Biol. 9 (8), e1001124.
Hanafy, A.H., Mishriky, J.F., Khalil, M.K., 2000. Reducing nitrate accumulation in
lettuce (Lactuca sativa L.) plants by using different biofertilizers. In:
Proceedings of the International Conference for Environmental Hazard
Mitigation, Cairo, Egypt, September.
Harada, H., Kuromori, T., Horayama, T., Shinozaki, K., Leig, R.A., 2004. Quantitative
trait loci analysis of nitrate storage in Arabidopsis leading to an investigation
of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate
levels. J. Exp. Bot. 55, 2005–2014.
Harrison, R., Webb, J., 2001. A review of the effect of N fertilizer type on gaseous
emissions. Adv. Agron. 73, 65–108.
Harrison, J., Hirel, B., Limani, A.M., 2004. Variation in nitrate uptake and
assimilation between two ecotypes of Lotus japojaponicas their recombinant
inbred lines. Physiol. Plant. 120, 124–131.
Hebbar, S.S., Ramachandrappa, B.K., Nanjappa, H.V., Prabhakar, M., 2004. Studies
on NPK drip fertigation in field grown tomato (Lycopersicon esculentum Mill.).
Eur. J. Agron. 21, 117–127.
Huett, D.O., 1996. Prospects for manipulating the vegetative-reproductive balance
in horticultural crops through nitrogen nutrition: a review. Aust. J. Agric. Res.
47, 47–66.
Jackson, D.I., Lombard, P.B., 1993. Environmental and management practices
affecting grape composition and wine quality—a review. Am. J. Enol. Vitic. 44,
409–430.
Ju, X., Liu, X., Zhang, F., Roelcke, M., 2004. Nitrogen fertilization, soil nitrate
accumulation, and policy recommendations in several agricultural regions of
China. Ambio 33, 300–305.
Kaiser, W.M., Huber, S.C., 1994. Posttranslational regulation of nitrate reductase in
higher plants. Plant Phys. 106, 817–821.
Kays, S.J., 1999. Preharvest factors affecting appearance. Postharvest Biol. Technol.
15, 233–247.
Konstantopoulou, E., Kapotis, G., Salachas, G., Petropoulos, S.A., Karapanos, I.C.,
Passam, H.C., 2010. Nutritional quality of greenhouse lettuce at harvest and
after storage in relation to N application and cultivation season. Sci. Hortic. 125
(93), e1-93.e5.
Koutinas, N., Pepelyankov, G., Lichev, V., 2010. Flower induction and flower bud
development in apple and sweet cherry. Biotechnol. Biotechnol. Equip. 24,
1549–1558.
Lairon, D., 2010. Nutritional quality and safety of organic food. A review. Agron.
Sustain. Dev. 30, 33–41.
Lillo, C., 1994. Light regulation of nitrate reductase in green leaves of higher plants.
Phys. Plant. 90, 616–620.
Maathuis, F.J.M., 2009. Physiological functions of mineral macronutrients. Curr.
Opin. Plant Biol. 12, 250–258.
Mattheis, J.P., Fellman, J.K., 1999. Preharvest factors influencing flavor of fresh fruit
and vegetables. Postharvest Biol. Technol. 15, 227–232.
McCall, D., Willumsen, J., 1999. Effects of nitrogen availability and supplementary
light on the nitrate content of soil-grown lettuce. J. Hortic. Sci. Biotechnol. 74,
458–463.
Melillo, E.D., 2012. The first green revolution: debt peonage and the making of the
nitrogen fertilizer trade 1840–1930. Am. Hist. Rev. 117, 1028–1060.
Mengel, K., Kirkby, E.A., Kosegarten, H., Appel, T., 2001. Principles of Plant
Nutrition. Kluwer Academic Publishers, Dordrecht.
Najera, F., Tapia, Y., Baginsky, C., Figueroa, V., Cabeza, R., Salazar, O., 2015.
Evaluation of soil fertility and fertilization practices for irrigation maize (Zea
mays L.) under Mediterranean conditions in Central Chile. J. Soil Sci. Plant Nutr.
15, 84–97.
Nielsen, G.H., Kappel, F., Nielsen, D., 2007. Fertigation and crop load affect yield,
nutrition, and fruit quality of ‘Lapins’ sweet cherry on Gisela 5 rootstock.
HortScience 42, 1456–1462.
Nielsen, G.H., Nielsen, D., Herbert, L., 2009. Nitrogen fertigation concentration and
timing of application affect nitrogen nutrition, yield, firmness, and color of
apples grown at high density. HortScience 44, 1425–1431.
Ombodi, A., Pesti, R., Balogh, A., Dimeny, J., Morikawa, C.K., Saigusa, M., 2010.
Reducing nitrate accumulation of different vegetables by controlled-release
fertilizer and chloride application. Acta Hortic. 938, 195–202.
Parisi, M., Giordano, L., Pentangelo, A., D’Onofrio, B., Villari, G., 2006. Effects of
different levels of nitrogen fertilization on yield and fruit quality in processing
tomato. Acta Hortic. 700, 129–132.
Reinink, K., Groenwold, R., Bootsma, A., 1987. Genotypical differences in nitrate
content in Lactuca sativa L. and related species and correlation with dry matter
content. Euphytica 36, 11–18.
Rembialkowska, E., 2007. Quality of plant products from organic agriculture. J. Sci.
Food Agric. 87, 2757–2762.
Riens, B., Heldt, H.W., 1992. Decrease of nitrate reductase activity in spinach leaves
during a light-dark transition. Plant Phys. 98, 573–577.
Rivas-Ubach, A., Sardans, J., Perez-Trujillo, M., Estiarte, M., Penuelas, J., 2012.
Strong relationship between elemental stoichiometry and metabolome in
plants. Proc. Natl. Acad. Sci. U. S. A. 109, 4181–4186.
83
Robertson, G.P., Vitousek, P.M., 2009. Nitrogen in agriculture: balancing the cost of
an essential resource. Ann. Rev. Environ. Res. 34, 97–125.
Ruiz, J.M., Romero, L., 1999. Cucumber yield and nitrogen metabolism in response
to nitrogen supply. Sci. Hortic. 82, 309–316.
Sams, C.E., 1999. Preharvest factors affecting postharvest texture. Postharvest Biol.
Technol. 15, 249–254.
Samuoliene, G., Urbonaviciute, A., Duchovskis, P., Bliznikas, Z., Vitta, P., Zukauskas,
A., 2009. Decrease in nitrate concentration in leafy vegetables under a
solid-state illuminator. HortScience 44, 1857–1860.
Santamaria, P., Elia, A., Gonnella, M., Parente, A., Serio, F., 2001. Ways of reducing
rocket salad nitrate content. Acta Hortic. 548, 529–537.
Santamaria, P., 2006. Nitrate in vegetables: toxicity, content, intake and EC
regulation. J. Sci. Food Agric. 86, 10–17.
Schenk, M.K., 2004. Agricultural practices to minimize nitrate accumulation in
edible parts of crop plants. In: Welch, R.M., Kakmak, I. (Eds.), Impacts of
Agriculture on Human Health and Nutrition, Encyclopedia of Life Support
Systems. EOLSS Publishers, Paris.
Schreiner, M., Korn, M., Stenger, M., Holzgreve, L., Altmann, M., 2013. Current
understanding and use of quality characteristics of horticultural products. Sci.
Hortic. 163, 63–69.
Sinclair, T.R., Rufty, T.W., 2012. Nitrogen and water resources commonly limit crop
yield increases, not necessarily plant genetics. Global Food Secur. 1, 94–98.
Smith, V.H., Tilman, G.D., Nekola, J.C., 1999. Eutrophication: impacts of excess
nutrient inputs on freshwater, marine and terrestrial ecosystems. Environ.
Pollut. 100, 179–196.
Smolen, S., Sady, W., 2009. The effect of various nitrogen fertilization and foliar
nutrition regimes on the concentrations of sugars, carotenoids and phenolic
compounds in carrot (Daucus carota L.). Sci. Hortic. 120, 315–324.
Stefanelli, D., Goodwin, I., Jones, R., 2010. Minimal nitrogen and water use in
horticulture: effects on quality and content of selected nutrients. Food Res. Int.
43, 1833–1843.
Stefanelli, D., Winkler, S., Jones, R., 2011. Reduced nitrogen availability during
growth improves quality in red oak lettuce leaves by minimizing nitrate
content, and increasing antioxidant capacity and leaf mineral content. Agric.
Sci. 2, 477–486.
Stitt, M., 1999. Nitrate regulation of metabolism and growth. Curr. Opin. Plant Biol.
2, 178–186.
Tagliavini, M., Zavalloni, C., Rombola, A.D., Quartieri, M., Malaguti, D., Mazzanti, F.,
Millard, P., Marangoni, B., 2000. Mineral nutrient partitioning to fruits of
deciduous trees. Acta Hortic. 512, 131–140.
Tilman, D., Cassman, K.G., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural
sustainability and intensive production practices. Nature 418, 671–677.
Tilman, D., 1998. The greening of the green revolution. Nature 396, 211–212.
Urrestarazu, M., Postigo, A., Salas, M., Sanchez, A., Carrasco, G., 1998. Nitrate
accumulation reduction using chloride in the nutrient solution on lettuce
growing by NFT in semiarid climate conditions. J. Plant Nutr. 21, 1705–1714.
Van Der Boon, J., Steenhuizen, J.W., 1986. Reduction of the nitrate concentration of
lettuce grown in recirculating nutrient solution. In: Lambers, H., Neetson, J.J.,
Stulen, I. (Eds.), Fundamental, Ecological and Agricultural Aspects of Nitrogen
Metabolism in Higher Plants. Springer, Netherlands.
Van Herwaarden, A.F., Farquhar, G.D., Angus, J.F., Richards, R.A., Howe, G.N., 1998.
‘Haying-off’, the negative grain yield response of dryland wheat to nitrogen
fertilizer. I. Biomass, grain yield, and water use. Aust. J. Agric. Res. 49,
1067–1081.
Wang, H., Cheng, L., 2011. Differential effects of nitrogen supply on skin
pigmentation and flesh starch breakdown of ‘Gala’ apple. HortScience 46,
1116–1120.
Wang, Z., Li, S., 2004. Effects of nitrogen and phosphorous fertilization on plant
growth and nitrate accumulation in vegetables. J. Plant Nutr. 27, 539–556.
Wang, Z., Li, S., Malhi, S., 2008. Effects of fertilization and other agronomic
measures on nutritional quality of crops. J. Sci. Food Agric. 88, 7–23.
Wang, D., Xu, Z., Zhao, J., Wang, Y., Yu, Z., 2011. Excessive nitrogen application
decreases grain yield and increases nitrogen loss in a wheat-soil system. Acta
Agric. Scand. B Soil Plant 61, 681–692.
Wanglai, Z., Wenke, L., Qichang, Y., 2013. Reducing nitrate content in lettuce by
pre-harvest continuous light delivered by red and blue light-emitting diodes. J.
Plant Nutr. 36, 481–490.
Wargo, J.M., Merwin, I.A., Watkins, C.B., 2003. Fruit size, yield, and market value of
‘GoldRush’ apple are affected by amount, timing and method of nitrogen
fertilization. HortTechnology 13, 153–161.
Weinbaum, S.A., Johnson, R.S., DeJong, T.M., 1992. Causes and consequences of
overfertilization in orchards. HortTechnology 2, 112–120.
Wilkie, J.D., Sedgley, M., Olesen, T., 2008. Regulation of floral initiaition in
horticultural trees. J. Exp. Bot. 59, 3215–3228.
Zhao, X., Carey, E.E., Wang, W., Rajashekar, C.B., 2006. Does organic production
enhance phytochemical content of fruit and vegetables? Current knowledge
and prospects for research. HortTechnology 16, 449–456.