ISSN 1807-1929

Revista Brasileira de Engenharia Agrícola e Ambiental

Brazilian Journal of Agricultural and Environmental Engineering
v.27, n.12, p.958-965, 2023
Campina Grande, PB – http://www.agriambi.com.br – http://www.scielo.br/rbeaa

DOI: http://dx.doi.org/10.1590/1807-1929/agriambi.v27n12p958-965

Morphophysiology and gas exchange of pomegranate

under salt stress and foliar application of nitrogen1
Morfofisiologia e trocas gasosas da romãzeira sob estresse salino
e aplicação foliar de nitrogênio
Francisco R. A. Figueiredo2 , Reynaldo T. de Fátima3 , Jackson S. Nóbrega3* , Toshik I. da Silva4 ,
Jean T. A. Ferreira3 , João E. da S. Ribeiro2 , Márcia P. da S. Leal5 ,
Lauriane A. dos A. Soares6 & Thiago J. Dias5
1
Research developed at Universidade Federal da Paraíba, Centro de Ciências Agrárias, Areia, PB, Brazil
2
Universidade Federal Rural do Semi-Árido/Programa de Pós-Graduação em Fitotecnia, Mossoró, RN, Brazil
3
Universidade Federal de Campina Grande/Programa de Pós-Graduação em Engenharia Agrícola, Campina Grande, PB, Brazil
4
Universidade Federal de Campina Grande/Programa de Pós-Graduação em Horticultura Tropical, Pombal, PB, Brazil
5
Universidade Federal da Paraíba/Programa de Pós-Graduação em Agronomia, Areia, PB, Brazil
6
Universidade Federal de Campina Grande/Centro de Ciências e Tecnologia Agroalimentar, Pombal, PB, Brazil

HIGHLIGHTS:
Salinity reduces growth and gas exchange of pomegranate.
Foliar-applied N dose of up to 1.31 g L-1 reduces the harmful effect of salinity on pomegranate growth.
Foliar nitrogen fertilization up to 1.59 g L-1 increases net photosynthesis.

ABSTRACT: Salinity is one of the abiotic stresses that affect gas exchange and growth of pomegranate. In this context,
the application of nitrogen fertilizer through the leaves can minimize these effects. Thus, the objective of present
study was to evaluate the effect of foliar nitrogen fertilization on pomegranate seedlings irrigated with brackish water.
The design used was randomized blocks, in an incomplete factorial scheme (Central Composite Design) with five
electrical conductivities of irrigation water - ECw (0.50, 1.15, 2.75, 4.35, and 5.00 dS m-1) and five doses of foliar
nitrogen fertilization - FNF (0, 0.33, 1.15, 1.97, and 2.30 g L-1), with four replicates and two plants per experimental
plot. Plant height, number of leaves, stem diameter, and gas exchange (stomatal conductance, net photosynthesis,
intercellular CO2 concentration, transpiration rate, instantaneous carboxylation efficiency, instantaneous water use
efficiency, and intrinsic water use efficiency) were evaluated at 60 days after the beginning of irrigation with saline
water. Salinity of irrigation water negatively affects the gas exchange of pomegranate seedlings. Foliar nitrogen
fertilization up to 1.31 g L-1 improves plant height and number of leaves in pomegranate seedlings under salt stress.
Foliar nitrogen fertilization up to 1.59 g L-1 increases the net photosynthesis of pomegranate seedlings.
Key words: Punica granatum L., photosynthesis, nitrogen, salinity

RESUMO: A salinidade é um dos estresses abióticos que afeta as trocas gasosas e o crescimento de romãzeira. Neste
sentido, à aplicação de adubo nitrogenado via foliar poderá minimizar estes efeitos. Com isso, o objetivo do presente
estudo foi avaliar o efeito da aplicação foliar com nitrogênio em mudas de romã irrigadas com águas salobra. O
delineamento utilizado foi de blocos casualizados, em esquema fatorial incompleto (Composto Central de Box),
sendo cinco condutividade elétrica da água - CEa (0,50; 1,15; 2,75; 4,35 e 5,00 dS m-1) e cinco doses de adubação
nitrogenada via foliar – ANF (0; 0,33; 1,15; 1,97 e 2,30 g L-1), com quatro repetições. A salinidade da água de irrigação
afeta negativamente as trocas gasosas de mudas de romãzeira. A adubação nitrogenada foliar até 1,31 g L-1 melhora o
crescimento em altura e no número de folhas em mudas de romãzeira sob estresse salino. Adubação nitrogenada
foliar até a dose de 1,59 g L-1 aumenta a fotossíntese das mudas de romãzeira.
Palavras-chave: Punica granatum L., fotossíntese, nitrogênio, salinidade

• Ref. 271570 – Received 28 Jan, 2023 This is an open-access article

* Corresponding author - E-mail: jacksonnobrega@hotmail.com distributed under the Creative
• Accepted 22 Jul, 2023 • Published 09 Aug, 2023 Commons Attribution 4.0
Editors: Ítalo Herbet Lucena Cavalcante & Hans Raj Gheyi International License.
 Morphophysiology and gas exchange of pomegranate under salt stress and foliar application of nitrogen 959

Introduction Material and Methods

Pomegranate (Punica granatum L.) is a fruit species native The experiment was conducted from April to August
to Iran, used as a functional source of food and nutraceuticals, 2019 in a greenhouse covered with semi-transparent plastic
and its cultivation is increasingly expanding in semiarid and with screened walls on the sides, with the seedlings
regions, where soil salinity is a limiting factor (Catola et al., arranged on masonry benches at 1.0 m from the floor, at the
2016). Short- and long-term salinity adversely affects the Agricultural Sciences Center of the Universidade Federal da
growth and physiological processes of this crop (Soares et Paraíba, Areia, Paraíba, Brazil. The municipality is located at
al., 2021), highlighting the need for techniques to minimize the geographical coordinates 6º 58’ 00’’ S and 35o 41’ 00’’ W
these effects. with an altitude of 575 m. The climate of the region, according
to Köppen’s classification, is of the As’ type, with dry and hot
Salinity is a serious problem in semiarid regions and
summer and rain in the winter (Alvares et al., 2013). The
irrigated areas, negatively affecting agricultural production.
data of temperature (maximum and minimum), relative air
Irrigation with brackish water favors the increase of toxic
humidity, and precipitation during the experimental period
ions such as sodium (Na+) and chloride (Cl-), resulting in
were collected daily and are presented in Figure 1.
decreased osmotic potential, interruption of morphological
The experimental design was in randomized blocks, in
and physiological processes, ionic toxicity and nutritional an incomplete factorial scheme (Central Composite Design),
imbalance of plants (Soares et al., 2021; Nóbrega et al., 2023). with five electrical conductivities (0.50, 1.15, 2.75, 4.35, and
Excessive absorption of these salts alters the hormonal 5.00 dS m-1) and five doses of foliar nitrogen fertilization (0,
balance and increases the production of reactive oxygen 0.33, 1.15, 1.97, and 2.30 g L-1), with four replicates and two
species, influencing growth and decreasing seedling quality plants per replicate, totaling nine combinations (Table 1).
(Bezerra et al., 2019). Salt stress negatively affects gas exchange, The treatments were determined from the Central Composite
causing a reduction in CO2 diffusion in the chloroplast due to Design generated from the formula: MNT = 2k + 2*k + 1,
stomatal restrictions, as well as photochemical changes and where, MNT = minimum number of treatments, k = number
carbon metabolism, and these effects may vary according to of factors.
the intensity and duration of stress (Lima et al., 2020).
N is the main essential element constituting amino acids Table 1. Representative scheme of the combinations and factors
(ECw - electrical conductivity of irrigation water; DFN - foliar
and proteins that protect the plant against abiotic stresses
nitrogen doses) used in the experiment
(Coulombier et al., 2020). The role of N against salt stress is
associated with the production of solutes, such as proline,
which maintains osmotic balance and protects cells against
reactive oxygen species (Cerqueira et al., 2019). The beneficial
effect of N has already been reported by some authors for
Malpighia emarginata applied to the soil (Lima et al., 2020), and
for Passiflora edulis (Pereira et al., 2022) and Anonna squamosa
L. (Fátima et al., 2023) by foliar application.
Thus, the objective of this study was to evaluate the effect of
foliar nitrogen fertilization on pomegranate seedlings irrigated ECw - Electrical conductivity of irrigation water; ND - Nitrogen doses; α - Distance
with saline water. between each axial point and the center in a central composite design

Figure 1. Data of maximum and minimum air temperature, precipitation, and average relative air humidity during the
experimental period in greenhouse

Rev. Bras. Eng. Agríc. Ambiental, v.27, n.12, p.958-965, 2023.

960 Francisco R. A. Figueiredo et al.

Pomegranate seeds cv. Mollar from fruits harvested in the Foliar nitrogen fertilization started at 25 DAE, with
orchard of the Universidade Federal Rural do Semi-Árido previous dissolution of the fertilizer in distilled water, followed
(UFERSA) were used. After acquiring the fruits, the seeds by application with an atomizer. In total, seven applications
were extracted and processed manually with the aid of a #¼ were performed, at interval of 10 days. The total volume applied
mesh sieve to remove the sarcotesta, to overcome the possible was 175 mL per plant, which provided 0, 58.16, 200, 341.84,
dormancy of the seeds, aiming at the standardization of and 400 mg of N per plant according to the increase of the
germination and the establishment of seedlings. Three seeds evaluated doses, based on study of Fátima et al. (2023).
were used per polyethylene bag, which was kept close to the The polyethylene bags had a capacity of 1.15 dm3, filled
field capacity from sowing to germination. Seed germination with substrate formed by 85% soil, 10% fine sand and 5% aged
began four days after sowing, extending to 25 days, when manure (Sakazaki et al., 2019). The physical and chemical
seedling emergence was established. At 25 days after sowing, characteristics of the substrate were evaluated according to
thinning was performed, leaving only one plant per bag, which methodologies proposed by EMBRAPA (2017) and Richards
was considered the most vigorous. (1954) (Table 2).
The electrical conductivities of irrigation water (ECw) The evaluations were carried out at 90 days after the
were obtained by dissolving sodium chloride (NaCl) in beginning of the treatment application. Gas exchange was
water from the supply system (0.5 dS m-1), until the required measured on the fourth leaf from the apex to the base, between
conductivities were obtained, the values being measured with a 9 and 10 a.m. with an infrared gas analyzer – IRGA (LI-6400XT,
microprocessor-based portable conductivity meter (model CD- LI-COR®, Nebraska, USA) with an air flow of 300 µmol s-1
860, Instrutherm®). The application of brackish water started 25 and humidity between 50-60%, 400 µmol mol-1 of CO2 and
days after emergence (DAE), with daily manual irrigation. The 1200 µmol m-2 s-1 coupled light source. Stomatal conductance
crop water demand was determined by the drainage lysimetry (gs – mol H2O m-2 s-1), net photosynthesis (A – μmol CO2 m-2
(Bernardo et al., 2019) method (Eq. 1), with the volume of s-1), intercellular CO2 concentration (Ci – mmol CO2 mol-1),
water lost through evapotranspiration the previous day being transpiration rate (E – mmol H2O m-2 s-1), instantaneous water
replaced daily, thus maintaining the soil at field capacity. use efficiency (WUE – [(μmol CO2 m-2 s-1) (mmol H2O m-2
s-1)-1]), intrinsic water use efficiency (iWUE - [(µmol CO2 m-2
( Va − Vd ) s-1) (mmol H2O m-2 s-1)-1]), and instantaneous carboxylation
VI = (1) efficiency (iCE – [(μmol CO2 m-2 s-1) (mmol CO2 mol-1)-1])
(1 − LF ) were evaluated.
To evaluate the growth of pomegranate seedlings, plant
where: height was analyzed, considering the distance from the collar
VI - volume of water to be used in the next irrigation (mL); to the apex of the plant, evaluated with a ruler graduated in
Va - volume of water applied in the previous irrigation cm; stem diameter was measured with a digital caliper and
event (mL); expressed in mm; and the number of leaves was determined
Vd - volume drained (mL); and, by counting fully formed leaves.
LF - leaching fraction (0.15). Data were subjected to normality (Shapiro-Wilk) and
homogeneity of variances (Bartlett) tests. Subsequently, an
Every 15 days a 15% leaching fraction was applied based analysis of variance (p ≤ 0.05) was performed, and a regression
on the volume applied in this period, in order to reduce the analysis was carried out in cases of significance. The statistical
accumulation of substrate salts. program R (R Core Team, 2021) was used.
Nitrogen doses were based on the need for 300 mg per
plant, proposed by Novais et al. (1991) for a 1 dm3 pot, the
Results and Discussion
highest evaluated dose being 400 mg per plant. The commercial
product Nitrotecnia-20 (Carbotecnia®), based on urea, with As observed in the summary of the analysis of variance
99 g L-1 of N, was used. (Table 3), a significant effect was found for the interaction

Table 2. Physical and chemical composition of the components of substrate used in the experiment

OM - Organic matter; SB - Sum of bases (Na+ + K+ + Ca2+ + Mg2+); CEC - Cation exchange capacity = SB + (H+ + Al3+); ECse - Electrical conductivity of the saturation extract;
SARse - Sodium adsorption ratio of the saturation extract = Na+ × [(Ca2+ + Mg2+)/2]1/2; ESP - Exchangeable sodium percentage (100 × Na+/CEC)

Rev. Bras. Eng. Agríc. Ambiental, v.27, n.12, p.958-965, 2023.

 Morphophysiology and gas exchange of pomegranate under salt stress and foliar application of nitrogen 961

Table 3. Summary of the analysis of variance for stomatal conductance (gs), net photosynthesis (A), intercellular CO2
concentration (Ci), instantaneous carboxylation efficiency (iCE), intrinsic water use efficiency (iWUE), instantaneous water
use efficiency (WUE), plant height (PH), number of leaves (NL), and stem diameter (SD) of Punica granatum L. under foliar
nitrogen fertilization (DFN) and salinity of brackish irrigation water (ECw)

* - Significant at p ≤ 0.05 and p ≤ 0.01, respectively; ns - Not significant, by F test

between brackish water and foliar nitrogen rates for water this efficiency is reduced. This behavior is a response to the
use efficiency - WUE, plant height - PH and number of leaves deleterious effects caused by salt stress, which induces this low
- NL. No significant effect was observed for the transpiration water consumption, limiting the absorption of toxic ions, as
variable - E. Individual effect was observed for the other observed by Nóbrega et al. (2022) in Mesosphaerum suaveolens.
analyzed variables (Table 3). The intrinsic water use efficiency (iWUE) increased up to
For stomatal conductance (gs) and net photosynthesis (A), the ECw of 2.20 dS m-1, reaching a value of 105.87 (Figure 2E).
there was a linear reduction as a function of the salinity of The greater iWUE observed in this study is associated with a
brackish irrigation water, with the highest values (0.076 mol plant mechanism of adaptation to stress conditions, leading to
m-2 s-1 and 7.142 μmol CO2 m-2 s-1, respectively) at the ECw of the maintenance of water in the tissues, as reported by Huang et
0.5 dS m-1, with decreases of 25.3 and 41.5%, at the highest al. (2015). The negative effects of salinity on gas exchange have
salinity of 5.00 dS m-1 (Figures 2A and 2B). The occurrence of been observed in plants of Solanum lycopersicum (Talebnejad &
these reductions is common in plants subjected to salt stress, Sepaskhah, 2016), Passiflora edulis (Silva et al., 2019), Psidium
closing their stomata as a defense mechanism of the plant. guajava L. (Bezerra et al., 2019), and Punica granatum L.
Consequently, CO2 absorption decreases, reducing the rate (Soares et al., 2021), results similar to those found in this study.
of net photosynthesis. This fact was observed by Soares et al. The foliar nitrogen fertilization promoted increases in
(2021) in pomegranate seedlings and by Silva et al. (2019) in gs, with the highest value obtained being 0.0747 mol m-2 s-1 at
yellow passion fruit, under saline conditions. the dose of 1.6 g L-1 of N, representing gains of 45.6% when
The intercellular CO2 concentration (Ci) was higher (277.70 compared to plants of the control treatment (dose 0), indicating
μmol CO2 m-2 s-1) in seedlings subjected to ECw of 0.5 dS m-1, the beneficial effect of foliar application of N on the gs of
followed by decreases up to ECw of 4.1 dS m-1 (232 μmol CO2 pomegranate plants (Figure 3A). This result may be related to
m-2 s-1), reaching decreases equivalent to 16.1% when compared the positive effect of nitrogen on plants, which is an important
to the values obtained in seedlings subjected to ECw of 0.5 dS component in the synthesis of photosynthetic pigments and
m-1 (Figure 2C). The reduction of Ci up to the salinity of 4.1 enzymes, as it improves stomatal regulation and the light
dS m-1 shows that the decrease in photosynthesis may be due saturation point, which explains the increases found for gs in
not only to stomatal factors, but also to factors of non-stomatal this study (Wang et al., 2016).
nature, such as biochemical alterations in the reduction of Foliar nitrogen fertilization stimulated A and Ci, with the
energy supply, which supposedly can affect the activity of highest values of 6.3457 and 270.26 μmol CO2 m-2 s-1 being
ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), observed at doses of 1.6 and 1.2 g L-1, representing gains
as reported by Sá et al. (2019). equivalent to 46.9 and 18.8%, respectively (Figures 3B and
The instantaneous carboxylation efficiency (iCE) was 3C). This positive effect indicates that the foliar application
reduced with increasing salinity, with the highest value (0.026) of nitrogen promoted improvements in the assimilation and
at the ECw of 0.5 dS m-1, followed by decreases that reached internal concentration of CO2 in pomegranate seedlings. This
36.1% at the salinity of 5.00 dS m-1 (Figure 2D). This marked can be explained by the fact that N is a nutrient that acts in
reduction in iCE with the increase in salinity levels is due to the several physiological processes, being involved in the synthesis
deleterious effects on the absorption and assimilation of CO2 of chlorophyll, influencing the photosynthetic capacity of the
by pomegranate seedlings. This directly reflects the reduction plant (Cerqueira et al., 2019).
of photosynthesis, promoting metabolic changes in the Calvin The intrinsic water use efficiency (iWUE) was reduced
cycle, preventing carbon from being fixed (Sousa et al., 2016). up to the dose of 1.47 g L-1 of N, increasing at the highest
The instantaneous water use efficiency (WUE) (Z = 3.46 concentrations (Figure 3D). The occurrence of this effect
– 0.13**x - 0.08**x2 - 0.18**y - 0.26**y2 + 0.29**xy; R2 = 0.54) may be associated with the positive effect of N on stomatal
was higher at the dose of 0.03 g L -1 of N and ECw of opening, as observed in gs, favoring the diffusion of CO2 in
0.52 dS m-1. The occurrence of this effect indicates that N the cells of the leaf mesophyll, consequently facilitating the loss
promotes improvements in WUE when pomegranate plants of water through transpiration, reducing water use efficiency
are subjected to high salinity, so when the ECw increases (Talebnejad & Sepakhah, 2016).

Rev. Bras. Eng. Agríc. Ambiental, v.27, n.12, p.958-965, 2023.

962 Francisco R. A. Figueiredo et al.

*, ** - Significant at p ≤ 0.05 and p ≤ 0.01, respectively; ns - Not significant, by F test

Figure 2. Stomatal conductance – gs (A), net photosynthesis – A (B), intercellular CO2 concentration – Ci (C), instantaneous
carboxylation efficiency – iCE (D), and instantaneous water use efficiency – iWUE (E) of Punica granatum L. under foliar
nitrogen fertilization and salinity of brackish irrigation water (ECw)

For the interaction between factors, foliar nitrogen nitrogen improves the performance of pomegranate seedlings.
fertilization and brackish water for plant height and number This is due to the fact that this nutrient is part of several organic
of leaves, foliar nitrogen fertilization at doses of 1.28 and compounds important for plant metabolism (amino acids,
1.31 g L-1 reduced the deleterious effects of salinity up to the proteins, proline), favoring osmotic adjustment (Cerqueira et al.,
ECw of 0.52 and 1.73 dS m-1, respectively (Figures 4A and 4B). 2019). Foliar nitrogen fertilization attenuates salt stress in yellow
The attenuating effect of nitrogen on growth in height and passion fruit seedlings – Passiflora edulis (Pereira et al., 2022)
number of leaves is an indication that foliar application of and sugar apple – Annona squamosa L. (Fátima et al., 2023).

Rev. Bras. Eng. Agríc. Ambiental, v.27, n.12, p.958-965, 2023.

 Morphophysiology and gas exchange of pomegranate under salt stress and foliar application of nitrogen 963

*, ** - Significant at p ≤ 0.05 and p ≤ 0.01, respectively; ns - Not significant, by F test *, ** - Significant at p ≤ 0.05 and p ≤ 0.01, respectively, by F test
Figure 3. Stomatal conductance - gs (A), net photosynthesis - Figure 4. Plant height (A), number of leaves (B) as a function of
A (B), intercellular CO2 concentration - Ci (C), and intrinsic interaction between foliar nitrogen fertilization and salinity of
water use efficiency - iWUE (D) of Punica granatum L. under irrigation water and stem diameter (C and D) of Punica granatum
foliar nitrogen fertilization L. under foliar nitrogen fertilization and salinity of irrigation water

Rev. Bras. Eng. Agríc. Ambiental, v.27, n.12, p.958-965, 2023.

964 Francisco R. A. Figueiredo et al.

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