Salicylic acid relieves the effect of saline stress on soursop morphysiology

Ácido salicílico alevia o efeito do estresse salino na morfofisiologia da gravioleira

André Alisson Rodrigues da Silva Geovani Soares de Lima Carlos Alberto Vieira de Azevedo Hans Raj Gheyi Allesson Ramos de Souza Pedro Dantas Fernandes About the authors

ABSTRACT

The cultivation of soursop has increased in recent years due to the advance of agribusiness and due to its use by the pharmaceutical industry. As a source of vitamin C, calcium, carbohydrates and antioxidant substances, soursop helps to protect the human body against oxidative stress, acting in the prevention of a series of chronic degenerative disorders. In this context, the objective of present study was to evaluate the effects of foliar sprays with salicylic acid to mitigate the effects of salt stress on the morphophysiology of soursop. The study was conducted in a greenhouse, in a randomized block design and a 5 × 4 factorial arrangement, with five levels of electrical conductivity of irrigation water - ECw (0.8-control; 1.6; 2.4; 3.2 and 4.0 dS m-1) and four concentrations of salicylic acid - SA (0; 1.2; 2.4 and 3.6 mM), with three replicates. Foliar application of SA at concentrations between 1.2 and 1.6 mM mitigated the effects of salt stress on stomatal conductance, CO2 assimilation rate, transpiration and instantaneous carboxylation efficiency of soursop at 480 days after transplanting. Spraying with SA at concentrations between 1.3 and 1.6 mM induced acclimatization to salt stress in soursop plants, since the percentage of intercellular electrolyte leakage was reduced and the growth was favored by the application of SA, even when exposed to salinity. Irrigation with ECw above 0.8 dS m-1 reduced the relative water content in the leaves of soursop cv. Morada Nova.

Index terms:
Annona muricata L; salinity; abiotic stress; elicitor.

RESUMO

O cultivo da graviola tem aumentado nos últimos anos em função do avanço da agroindústria e pela utilização na indústria farmacêutica. Em razão da fruta ser fonte de vitamina C, cálcio, carboidratos e substâncias antioxidantes, além de auxiliar na proteção contra o estresse oxidativo, atuando na prevenção de uma série de distúrbios crônico degenerativos. Nesse contexto, objetivou-se avaliar os efeitos de pulverizações foliares com o ácido salicílico na mitigação dos efeitos do estresse salino na morfofisiologia da gravioleira. O estudo foi conduzido em casa de vegetação, no delineamento de blocos casualizados e arranjo fatorial 5 × 4, com cinco níveis de condutividade elétrica da água de irrigação - CEa (0,8-controle; 1,6; 2,4; 3,2 e 4,0 dS m-1) e quatro concentrações de ácido salicílico - AS (0; 1,2; 2,4 e 3,6 mM), com três repetições. A aplicação foliar do AS entre as concentrações de 1,2 e 1,6 mM amenizou os efeitos do estresse salino sobre a condutância estomática, a taxa de assimilação de CO2, a transpiração e a eficiência instantânea da carboxilação da gravioleira aos 480 dias após o transplantio. A pulverização com AS com concentrações entre 1,3 e 1,6 mM induziu a aclimatação ao estresse salino na gravioleira, visto que, as plantas tiveram a porcentagem de extravasamento de eletrólitos reduzidos e o crescimento beneficiado pela aplicação de AS, mesmo quando expostas a salinidade. A irrigação com CEa acima de 0,8 dS m-1 reduziu o teor relativo de água nas folhas da gravioleira cv. Morada Nova.

Termos para indexação:
Annona muricata L; salinidade; estresse abiótico; elicitor.

INTRODUCTION

Salinity is one of the worst abiotic stresses that threaten agricultural production in the 21st century, and its adverse effects are expected to increase due to the climate change in recent years, especially in semi-arid regions (Ahmadi; Souri, 2018AHMADI, M.; SOURI, M. K. Growth and mineral elements of coriander (Corianderum sativum L.) plants under mild salinity with different salts. Acta Physiologia Plantarum, 40(1):94-99, 2018.; Souana et al., 2020SOUANA, K. et al. Salt-tolerance in Vicia faba L. is mitigated by the capacity of salicylic acid to improve photosynthesis and antioxidant response. Scientia Horticulturae , 273(1):e109641, 2020.).

The difficulty for the expansion of crops irrigated with saline water is related to the damage caused by the combination of osmotic and ionic stresses, which restricts the absorption of water and nutrients and consequently, affects physiological processes and plant growth (Ahmadi; Souri, 2020AHMADI, M.; SOURI, M. K. Growth characteristics and fruit quality of chili pepper under higher electrical conductivity of nutrient solution induced by various salts. Journal of Agricultural Science, 42(1):143-152, 2020.). Salt stress also causes oxidative stress due to the imbalance between the production of reactive oxygen species (ROS) and their detoxification by enzymatic and non-enzymatic reactions (Mohamed et al., 2020MOHAMED, I. A. A. et al. Stomatal and photosynthetic traits are associated with investigating sodium chloride tolerance of Brassica napus L. cultivars. Plants, 9(1):1-19, 2020.).

Given the increasing need to use saline water in irrigated agriculture, studies that enable the use of these sources of water have become indispensable. In this context, the use of salicylic acid - SA has emerged to minimize the harmful effects caused by abiotic stresses such as salinity (Nazar et al., 2015NAZAR, R. et al. Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. South African Journal of Botany , 98(1):84-94, 2015.).

Salicylic acid is a natural phenolic compound, which is involved in plant growth and physiological processes such as floral induction, stomatal opening and closure, ion absorption, photosynthesis and transpiration (Silva et al., 2020SILVA, A. A. R. et al. Salicylic acid as an attenuator of salt stress in soursop. Revista Caatinga , 33(4):1092-1101, 2020.). The beneficial effect of SA on different plant species under salt stress may arise from its role in intensifying the activity of antioxidant enzymes and in protecting membranes against damage (Esan et al., 2017ESAN, A. M. et al. Comparative effects of indole acetic acid and salicylic acid on oxidative stress marker and antioxidant potential of okra (Abelmoschus esculentus) fruit under salinity stress. Scientia Horticulturae, 216:278-283, 2017.). Souri and Tohidloo (2019SOURI, M. K.; TOHIDLOO, G. Effectiveness of different methods of salicylic acid application on growth characteristics of tomato seedlings under salinity. Chemical and Biological Technologies in Agriculture , 6:26, 2019.) has shown recently that the time and the method of application as well as the concentration of SA can significantly influence plant responses under salinity.

It has been reported that foliar spraying with SA can mitigate the deleterious effects caused by salt stress on strawberry (Samadi; Habibi; Varziri, 2019SAMADI, S.; HABIBI, G.; VAZIRI, A. Effects of exogenous salicylic acid on antioxidative responses, phenolic metabolism and photochemical activity of strawberry under salt stress. Iranian Journal of Plant Physiology , 9(2):2685-2694, 2019.), almond (Mohammadi et al., 2020MOHAMMADI, H. et al. Exogenous salicylic acid attenuates the adverse effects of salinity on some parameters related to photosynthesis of almond. Journal of Agricultural Science and Technology, 22(2):519-534, 2020.), grapes (Ekbic; Ozican; Erdem, 2020EKBIC, H. B.; OZCAN, N.; ERDEM, H. Impacts of salicylic acid treatments on salt resistance of some American grapevine rootstocks. Fresenius Environmental Bulletin, 29(2):685-692, 2020.), dates (Jasim; Ati, 2020JASIM, N. S.; ATI, M. A. A. Effect of salycilic acid on antioxidant enzymes and biochemical contents of date palm plantlets (Phoenix dactylifera L.) under salt stress conditions. Indian Journal of Ecology, 47(2):378-382, 2020.) and orange (Mahmoud et al., 2021MAHMOUD, L. M. et al. The response of salt-stressed Valencia sweet orange (Citrus sinensis) to salicylic acid and methyl jasmonate treatments. Plant Physiology Reports, 26:1-15, 2021.). However, information on its use in the soursop crop irrigated with saline waters is scarce.

Soursop (Annona muricata L.) is one of the most important fruit species of the Annonaceae family (Sánchez et al., 2018SÁNCHEZ, C. F. B. et al. Genetic diversity among soursop genotypes based on fruit production. Bioscience Journal, 34(1):122-128, 2018.). Its fruits are appreciated for their succulence, sweet and sub-acid flavor, as well as the pleasant and distinct aroma; its consumption, either fresh or processed, has increased due to its nutritional value and different forms of use in human food (Freitas et al., 2013FREITAS, A. L. G. E. de et al. Caracterização da produção e do mercado da graviola (Annona muricata L.) no estado da Bahia. Informações Econômicas, 43(1):23-34, 2013.; Jimenez et al., 2014JIMENEZ, V. M. et al. Identification of phenolic compounds in soursop (Annona muricata L.) pulp by high-performance liquid chromatography with diode array and electrospray ionization mass spectrometric detection. Food Research International, 65(1):42-46, 2014.; Leite Neta et al., 2019LEITE NETA, M. T. S. et al. Effect of spray drying on bioactive and volatile compounds in soursop (Annona muricata) fruit pulp. Food Research International , 124:70-77, 2019.). Apart from the medicinal properties of its leaves, fruits, seeds, and roots (Moghadamtousi et al., 2015MOGHADAMTOUSI, S. Z. et al. Annona muricata (Annonaceae): A review of its traditional uses, isolated acetogenins and biological activities. International Journal of Molecular Sciences, 16(7):15625-15658, 2015.).

In view of the above, the aim of this study was to evaluate the effects of foliar spraying with salicylic acid on the mitigation of salt stress and on the morphophysiology of soursop cv. Morada Nova.

MATERIAL AND METHODS

The experiment was carried out from June 2019 to October 2020, in a protected environment (greenhouse), belonging to the Academic Unit of Agricultural Engineering - UAEA of the Federal University of Campina Grande - UFCG, located in Campina Grande, Paraíba, Brazil, at the geographical coordinates 7°15’18” South latitude, 35°52’28” West longitude and mean altitude of 550 m. Data of temperature (maximum and minimum) and mean relative air humidity during the experimental period are shown in Figure 1.

Figure 1:
Air temperature (maximum and minimum) and mean relative air humidity observed in the internal area of the greenhouse during the experimental period.

The treatments consisted of five levels of electrical conductivity of irrigation water - ECw (0.8- control; 1.6, 2.4, 3.2 and 4.0 dS m-1) and four concentrations of salicylic acid - SA (0; 1.2, 2.4 and 3.6 mM), in a 5×4 factorial arrangement, distributed in randomized blocks, with three replicates, totaling 60 experimental units.

Salicylic acid concentrations studied were based on a study conducted by Abbaszadeh et al. (2020ABBASZADEH, B. et al. Improving water use efficiency through drought stress and using salicylic acid for proper production of Rosmarinus officinalis L. Industrial Crops and Products, 144:e111893, 2020. ) and ECw levels were according to results reported by Veloso et al. (2019VELOSO, L. L. S. A. et al. Effects of saline water and exogenous application of hydrogen peroxide (H2O2) on soursop (Annona muricata L.) at vegetative stage. Australian Journal of Crop Science, 13(3):472-479, 2019.).

The soursop cultivar ‘Morada Nova’ was chosen because it is the most appreciated by producers, making up most commercial orchards in Brazil, besides having larger fruits, which can weigh up to 15 kg, and higher production compared to other cultivars (São Jose et al., 2014SÃO JOSÉ, A. R. et al. Atualidades e perspectivas das Anonáceas no mundo. Revista Brasileira de Fruticultura, 36(1):86-93, 2014.). The seedlings were propagated sexually and their formation period was 330 days. After this period, they were transplanted to plastic pots of 120-L capacity.

The experiment was conducted adopting plastic containers as drainage lysimeters, filled with a 1.0-kg layer of crushed stone followed by 160 kg of soil classified as Entisol (United States, 2014UNITED STATES - Department of Agriculture. Keys to soil taxonomy. Natural Resources Conservation Service, 2014. 372p.), of 0-0.30 m depth, from the municipality of Lagoa Seca-PB, whose physico-chemical characteristics (Table 1) were determined according to Teixeira et al. (2017TEIXEIRA, P. C. et al. Manual de métodos de análise de solo. 3.ed., Brasília: Embrapa Solos, 2017. 573p.).

Table 1:
Chemical and physical attributes of the soil, in the 0-0.30 m depth, used in the experiment, before the application of the treatments.

The irrigation waters with different levels of electrical conductivity were prepared by dissolving NaCl, CaCl2.2H2O and MgCl2.6H2O salts, in the equivalent proportion of 7:2:1, respectively, in water from the local supply system (ECw = 0.38 dS m-1). This proportion is commonly found in sources of water used for irrigation in the Northeast region (Medeiros et al., 2003MEDEIROS, J. F. et al. Caracterização das águas subterrâneas usadas para irrigação na área produtora de melão da Chapada do Apodi. Revista Brasileira de Engenharia Agrícola e Ambiental , 7(3):469-472, 2003.). The irrigation waters were prepared considering the relationship between ECw and salt concentration (Richards, 1954RICHARDS, L. A. Diagnosis and improvement of saline and alkali soils. Washington: U.S. Department of Agriculture USDA Handbook 60. 1954. 160p.), according to Equation 1:

Q mmol c L 1 = 10 x ECw dS m 1 (1)

Where:

Q - amount of salts to be added (mmolc L-1)

ECw - electrical conductivity of water (dS m-1)

At 75 days after transplanting (DAT), irrigation with saline water began, adopting an interval of 3 days and applying water in each lysimeter according to the treatments, in order to maintain soil moisture close to field capacity. The volume of water to be applied was determined according to the water requirement of the plants, estimated by water balance, and was given by Equation 2:

VI = Va Vd 1 LF (2)

Where:

VI - volume of water to be used in the irrigation event (mL);

Va - volume applied in the previous irrigation event (mL);

Vd - volume drained (mL);

LF - leaching fraction of 0.15, applied every 30 days to avoid excessive accumulation of salts.

The concentrations of SA were obtained by dissolving the product in 30% ethyl alcohol (95.5%), as it is a substance of low solubility in water at room temperature. To reduce the surface tension of the drops on the leaf surface, the adjuvant Wil fix (0.5 mL L-1) was used in the preparation of the solution.

Foliar applications began at 60 DAT, on the abaxial and adaxial sides of the leaves. Subsequent applications were performed at 30-day intervals using a backpack sprayer between 17:00 and 17:45 h. The sprayer used is a model from Jacto - Jacto XP with capacity of 12 L, working pressure (maximum) of 88 psi (6 bar) and JD 12P nozzle, and the mean volume applied per plant was 400 mL.

Fertilization with nitrogen, phosphorus and potassium was based on the recommendations proposed by Cavalcante et al. (2008CAVALCANTE, F. J. A. et al. Recomendação de adubação para o Estado de Pernambuco: 2ª aproximação. 3.ed., Recife: Instituto Agronômico de Pernambuco, 2008. 212p.) for soursop crop, with 100 g of nitrogen, 60 g of P2O5 and 40 g of K2O per plant per year, split into 24 portions and applied at 15-day intervals. Urea, monoammonium phosphate and potassium chloride were used as sources of nitrogen, phosphorus and potassium, respectively.

A Dripsol® Micro solution, at the concentration of 1.0 g L-1, was applied every two weeks to meet the micronutrient requirement (composition: Mg (1.1%); Zn (4.2%); B (0.85%); Fe (3.4%); Mn (3.2%); Cu (0.5%); Mo (0.05%)), sprayed on the adaxial and abaxial sides of the leaves using a backpack sprayer. During the experiment, cultural practices such as cleaning pruning, weeding, soil scarification and the phytosanitary control recommended for the crop were performed as and when necessary.

At 480 DAT, the following parameters were evaluated: relative water content; percentage of intercellular electrolyte leakage (% IEL); gas exchange - stomatal conductance (gs), transpiration (E), CO2 assimilation rate (A), internal CO2 concentration (Ci), instantaneous water use efficiency (WUEi) (A/E) and instantaneous carboxylation efficiency (CEi) (A/Ci); and the growth variables - crown height (HCrown), stem diameter (SD), crown diameter (DCrown), crown volume (VCrown) and vegetative vigor index (VVI).

To determine the relative water content (RWC), two leaves were removed from the middle third of the main branch to obtain five discs of 12 mm of diameter from each leaf. Immediately after collection, the discs were weighed, avoiding moisture loss, obtaining the fresh mass (FM); then, these samples were placed in beaker, immersed in 50 mL of distilled water and conditioned for 90 minutes. After this period, excess water from the discs was removed with paper towels and the turgid mass (TM) of the samples was obtained, which were then dried in an oven at temperature ≈ 65 ± 3 ºC, until constant weight to obtain the dry mass (DM) of the samples. The RWC was determined according to Lima et al. (2015LIMA, G. S. de. et al. Water relations and gas exchange in castor bean irrigated with saline water of distinct cationic nature. African Journal of Agricultural Research, 10(13):1581-1594, 2015.), by Equation 3:

RWC = FM DM TM MS x 100 (3)

The percentage of intercellular electrolyte leakage (% IEL) was determined using a copper hole puncher to obtain five leaf discs with an area of 1.54 cm2 each, per experimental unit, which were washed and placed in Erlenmeyer® flask containing 50 mL of distilled water. After being closed with aluminum foil, the Erlenmeyer® flasks were kept at temperature of 25 °C for 90 minutes and then the initial electrical conductivity of the medium (Xi) was measured using a benchtop conductivity meter (MB11, MS Techonopon®). Then, the Erlenmeyer® flasks were subjected to a temperature of 90 °C for 90 minutes in a drying oven (SL100/336, SOLAB®) and, after cooling of their contents, the final conductivity (Xf) was measured. The percentage of intercellular electrolyte leakage was expressed as the percentage of initial electrical conductivity relative to the electrical conductivity after treatment for 90 minutes at 90 ºC: [(Xi/Xf) x 100] (Scotti-Campos et al., 2013SCOTTI-CAMPOS, P. et al. Physiological responses and membrane integrity in three Vigna genotypes with contrasting drought tolerance. Emirates Journal of Food and Agriculture, 25(12):1002-1013, 2013.).

Gas exchange was measured on the third leaf, counted from the apex of the main branch of the plant, using irradiation of 1200 μmol photons m-2 s-1 and airflow of 200 mL min-1, using the portable photosynthesis meter LCPro+ from ADC BioScientific Ltda.

HCrown was measured by taking as reference the distance from the plant collar to the insertion of the apical meristem; SD was measured at 3 cm height from the plant collar with a digital caliper; DCrown was obtained by mean of crown diameter observed in the directions of the planting row (DR) and inter-row (DIR); VCrown was calculated from HCrown, DR and DIR, using Equation 4; and VVI was obtained using Equation 5, according to Portella et al. (2016PORTELLA, C. R. et al. Desempenho de cultivares de citros enxertadas sobre o trifoliateiro ‘Flying Dragon’ e limoeiro ‘Cravo’ em fase de formação do pomar. Bragantia, 75(1):70-75, 2016.).

V Crown = π 6 x H Crown x DR x DIR (4)

VVI = H Crown + D Crown + SD x 10 100 (5)

Where:

VCrown - crown volume (m3);

DCrown - crown diameter (m);

VVI - vegetative vigor index;

HCrown - crown height (m);

DR - crown diameter in the direction of the row (m);

DIR - crown diameter in the direction of the inter-row (m); and,

SD - stem diameter (mm).

The data were subjected to the distribution normality test (Shapiro-Wilk test) at 0.05 probability level. Subsequent analysis of variance was performed at 0.05 and 0.01 probability level and, in cases of significance, linear and quadratic regression analysis was performed using the statistical program SISVAR-ESAL (Ferreira, 2019FERREIRA, D. F. SISVAR: A computer analysis system to fixed effects split plot type designs. Revista Brasileira de Biometria, 37(4):529-535, 2019. ). The choice of the model was made based on the significance of the coefficients. In case of significance of the interaction between factors, TableCurve 3D software was used to construct the response surfaces.

RESULTS AND DISCUSSION

There was significant interaction (p<0.01) between salinity levels (SL) and salicylic acid (SA) concentrations only for the percentage of intercellular electrolyte leakage (Table 2). The relative water content (RWC) was significantly affected by both factors individually.

Table 2:
Summary of the analysis of variance for relative water content (RWC) and percentage of intercellular electrolyte leakage (% IEL) of soursop cv. ‘Morada Nova’ cultivated with saline waters and foliar application of salicylic acid, at 480 days after transplanting.

The relative water content was reduced linearly with the increase in the electrical conductivity of irrigation water (Figure 2A), by 3.9% per unit increase in ECw. A reduction of 13.0% was observed when comparing the RWC of plants irrigated with water of highest salinity (4.0 dS m-1) to that of plants cultivated under the lowest salinity level (0.8 dS m-1). RWC is a variable that indicates the plant’s water status, and its reduction as a result of salinity may occur due to osmotic effects, which restricts the absorption of water by plants or due to enhancement in leaf transpiration rates (Morais et al., 2018MORAIS, M. B. de. et al. Multiple stresses on the oxidative metabolism of sugarcane varieties. Ciência Rural, 48(4):e20141487, 2018.; Ahmadi; Souri, 2019AHMADI, M.; SOURI, M. K. Nutrient uptake, proline content and antioxidant enzymes activity of pepper (Capsicum annuum L.) under higher electrical conductivity of nutrient solution created by nitrate or chloride salts of potassium and calcium. Acta Scientiarum Polonorum Hortorum Cultus, 18(5):113-122, 2019.; Hatamian et al., 2020HATAMIAN, M. et al. Interaction of lead and cadmium on growth and leaf morphophysiological characteristics of European hackberry (Celtis australis) seedlings. Chemical and Biological Technologies in Agriculture, 7(1):1-8, 2020.).

Figure 2:
Relative water content - RWC of soursop cv. ‘Morada Nova’ as a function of the electrical conductivity of irrigation water - ECw (A) and concentrations of salicylic acid - SA (B); and response surface for the percentage of intercellular electrolyte leakage - % IEL (C) as a function of the interaction between ECw and concentrations of SA, at 480 days after transplanting. X and Y - ECw and SA concentration, respectively; *, ** Significant at p ≤ 0.05 and at p ≤ 0.01, respectively. The point and vertical lines represent Mean +/- Standard Error (n=3).

In research conducted by Silva Neta et al. (2021SILVA NETA, A. M. D. S. et al. Morphophysiology of the passion fruit ‘BRS Rubi do Cerrado’ irrigated with saline waters and nitrogen fertilization. Comunicata Scientiae, 12(1):e3456, 2021.), evaluating the morphophysiology of ‘BRS Rubi do Cerrado’ passion fruit irrigated with saline water (0.3 to 3.5 dS m-1), also observed a reduction in RWC corresponding to 2.91% per unit increase in electrical conductivity.

Salicylic acid concentrations influenced the RWC of soursop (Figure 2B). Plants subjected to the concentration of 1.45 mM stood out with the highest value of RWC (84.3%) showing an increase of 8.8% compared to those grown under control treatment (without SA application). Such a response may be related to the effect of SA on the accumulation of osmolytes, which contribute to the reduction of osmotic potential, ensuring greater water absorption and an increase in the relative water content of tissues (Pooja; Sharma, 2016POOJA, D.; SHARMA, K. D. Salicylic acid induced amelioration of salinity stress in mungbean. Saarbrücken: Scholar‘s Press, 2016. 108p.).

For % IEL (Figure 2C), it was verified that the SA concentration of 1.3 mM mitigated the adverse effects of salinity, with the lowest % IEL value (25.78%) obtained in plants irrigated with 0.8 dS m-1 water. On the other hand, the plants in the control treatment (0 mM SA) when irrigated with 0.8 dS m-1 water showed % IEL of 27.43%, that is, an increase of 6.4% in comparison to plants subjected to a concentration of 1.3 mM.

The positive effects of SA in reducing percentage of intercellular electrolyte leakage of soursop can be attributed to the improvement in nutrient absorption, membrane protection and increase in photosynthetic activity. In addition, SA can interact with signaling pathways of reactive oxygen species (ROS) and reduce oxidative stress (Herrera-Vásquez; Salinas; Holuigue, 2015HERRERA-VÁSQUEZ, A.; SALINAS, P.; HOLUIGUE, L. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Frontiers in Plant Science, 6(1):171-179, 2015.; Batista et al., 2019BATISTA, V. C. V. et al. Salicylic acid modulates primary and volatile metabolites to alleviate salt stress-induced photosynthesis impairment on medicinal plant Egletes viscosa. Environmental and Experimental Botany, 167:e103870, 2019.).

It is worth mentioning that the increase in the electrical conductivity of irrigation water associated with SA concentrations greater than 1.3 mM intensified the deleterious effects of salinity on the percentage of intercellular electrolyte leakage, with the highest % IEL (34.79%) obtained in plants irrigated with 4.0 dS m-1 water and under SA concentration of 3.6 mM.

This response can be explained by the fact that salt stress induces the production of ROS, due to the reduction of light absorption and the electron transport chain, causing photooxidative damage to photosystems (Yudina et al., 2020YUDINA, L. et al. A light-induced decrease in the photochemical reflectance index (PRI) can be used to estimate the energy-dependent component of non-photochemical quenching under heat stress and soil drought in pea, wheat, and pumpkin. Photosynthesis Research, 146:175-187, 2020.), peroxidation of the cell membrane and increased percentage of intercellular electrolyte leakage.

According to the summary of the analysis of variance (Table 3), the interaction between SL and SA concentrations significantly influenced all gas exchange variables analyzed, except for the internal CO2 concentration and instantaneous water use efficiency. Salinity levels, on the other hand, significantly (p<0.01) affected the parameters Ci, gs, E, A and CEi. Salicylic acid concentrations caused significant effects on gs, A, CEi and WUEi. Besides this, significant effect of blocks was also observed on Ci, gs, A, CEi and WUEi, provoked perhaps due to differences in lumonisidade and temperature in the relatively large size (20 x 28m) of greenhouse.

Table 3:
Summary of the analysis of variance for the internal CO2 concentration (Ci), stomatal conductance (gs), transpiration (E), CO2 assimilation rate (A), instantaneous carboxylation efficiency (CEi) and instantaneous water use efficiency (WUEi) of soursop cv. ‘Morada Nova’ irrigated with saline waters and under foliar application of salicylic acid, at 480 days after transplanting.

The increase in the ECw caused a positive linear effect on the internal CO2 concentration (Figure 3), with an increment of 5.1% per unit increase in ECw. Plants irrigated with water of highest salinity (4.0 dS m-1) had an increase of 15.7% (30.4 μmol m-2 s-1), compared to those cultivated under ECw of 0.8 dS m-1. The increase in the internal concentration in the substomatic chamber in plants grown under salt stress is indicative of deterioration of the photosynthetic apparatus, as the damage caused to the structures responsible for CO2 fixation is not only due to stomatal factors, but also to the accumulation of salts in the leaves (Hussain et al., 2012HUSSAIN, S. et al. Physiological analysis of salt stress behavior of citrus species and genera: Low chloride accumulation as an indicator of salt tolerance. South African Journal of Botany, 81:103-112, 2012.). The increase in the internal concentration of CO2 due to the increase in salinity was also observed in other crops, such as West Indian cherry (Dias et al., 2018DIAS, A. S. et al. Gas exchanges and photochemical efficiency of West Indian cherry cultivated with saline water and potassium fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental, 22(9):628-633, 2018.), passion fruit (Lima et al., 2020LIMA, G. S. de. et al. Gas exchange, chloroplast pigments and growth of passion fruit cultivated with saline water and potassium fertilization. Revista Caatinga, 33(1):184-194, 2020.) and pomegranate (Soares et al., 2021SOARES, L. A. A. et al. Physiological changes of pomegranate seedlings under salt stress and nitrogen fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental , 25(7):453-459, 2021.).

Figure 3:
Internal CO2 concentration - Ci of soursop cv. ‘Morada Nova’ as a function of the electrical conductivity of irrigation water - ECw, at 480 days after transplanting. ** Significant at p ≤ 0.01. The point and vertical lines represent Mean +/- Standard Error (n=3).

Soursop plants irrigated with water of 1.4 dS m-1 and subjected to a SA concentration of 1.2 mM obtained the highest value of gs (0.083 mol H2O m-2 s-1) (Figure 4A), which corresponded to an increase of 5.2% (0.004 mol H2O m-2 s-1) in comparison to plants under control treatment (0 mM) irrigated using water with the same salinity level. However, SA concentrations above 1.2 mM associated with the increase in ECw led to a reduction in gs, with the lowest value (0.031 mol H2O m-2 s-1) being obtained in plants subjected to SA concentration of 3.6 mM and irrigated with water of 4.0 dS m-1.

Figure 4:
Response surface for stomatal conductance - gs (A), transpiration - E (B), CO2 assimilation rate - A (C) and instantaneous carboxylation efficiency - CEi (D) of soursop cv. Morada Nova as a function of the interaction between the electrical conductivity of irrigation water - ECw and the concentrations of salicylic acid, at 480 days after transplanting. X and Y - ECw and SA concentration, respectively; *, ** Significant at p ≤ 0.05 and at p ≤ 0.01, respectively.

Under conditions of salt stress, plants can close their stomata in response to the decrease in the relative water content in the leaves (Figure 2A) due to the osmotic effect. Under stress conditions, the reduction of gs is a defense mechanism of the plant to minimize the loss of water by the leaves to the atmosphere and, consequently, the absorption of water and salts from the soil solution (Hussain et al., 2012HUSSAIN, S. et al. Physiological analysis of salt stress behavior of citrus species and genera: Low chloride accumulation as an indicator of salt tolerance. South African Journal of Botany, 81:103-112, 2012.). Despite the reduction of stomatal conductance in plants under the highest salinity level (4.0 dS m-1), there was no restriction on the internal CO2 concentration (Figure 3).

In a study conducted by Khoshbakht and Asgharei (2015KHOSHBAKHT, D.; ASGHAREI, M. R. Influence of foliar-applied salicylic acid on growth, gas-exchange characteristics, and chlorophyll fluorescence in citrus under saline conditions. Photosynthetica, 53(3):410-418, 2015.), evaluating the influence of SA (0 to 1 mM) applied through the leaves on the growth, gas exchange and chlorophyll fluorescence of citrus under saline conditions (0 to 75 mM of NaCl), it was verified that the application of SA at the concentration of 1.0 mM promoted a higher degree of stomatal opening compared to the control treatment.

Salicylic acid at concentrations of up to 1.4 mM promoted an increase in E and A, regardless of the electrical conductivity of irrigation water (Figure 4B and 4C). It was observed that plants subjected to SA concentration of 1.4 mM and irrigated with water of 1.6 dS m-1 obtained higher values of E (2.17 mmol H2O m-2 s-1) and A (7.7 mmol CO2 m-2 s-1). Soursop plants irrigated with water of 1.6 dS m-1 and subjected to SA concentration of 1.4 mM increased by 7.8% (0.16 mmol H2O m-2 s-1) and 6.8% (0.49 mmol CO2 m-2 s-1) their E and A, respectively, compared to those cultivated under ECw of 1.6 dS m-1 and without application of SA (0 mM).

Similar results were obtained by Mohammadi et al. (2020MOHAMMADI, H. et al. Exogenous salicylic acid attenuates the adverse effects of salinity on some parameters related to photosynthesis of almond. Journal of Agricultural Science and Technology, 22(2):519-534, 2020.), evaluating the effect of foliar spraying of SA (0 to 2 mM) on almond plants (Prunus amygdalus L.) under salt stress (0 to 8 dS m-1); these authors observed that the application of SA at concentration of 1 mM mitigated the deleterious effects of salinity on the stomatal conductance, transpiration and CO2 assimilation rate of plants.

Salicylic acid helps in the protection and increase in the activity of antioxidant enzymes under stressful conditions, making plants tolerant to stress (Rajeshwari; Bhuvaneshwari, 2017RAJESHWARI, V.; BHUVANESHWARI, V. Salicylic acid induced salt stress tolerance in plants. International Journal of Plant Biology and Research, 5(3):1067-1073, 2017.). Under conditions of salt stress, SA can cause decrease of Na+ and Cl- ions and increase of the K+/Na+ ratio, improving photosynthetic activity (Gunes et al., 2007GUNES, A. et al. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology, 164(6):728-736, 2007.; Tufail et al., 2013TUFAIL, A. et al. Salicylic acid induced salinity tolerance in maize (Zea mays L.). Pakistan Journal of Botany, 45(1):75-82, 2013.). According to Nahar et al. (2016NAHAR, K. et al. Polyamines confer salt tolerance in mung bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Frontiers in Plant Science , 7:e1104, 2016.), the substitution of Na+ by K+, exclusion of Na+ and retention of intracellular K+ are important mechanisms for plant tolerance to salt stress.

For CEi (Figure 4D), it was verified that SA concentrations 1.6 mM and irrigation water salinity from 1.3 dS m-1 had a negative influence, with the lowest value of CEi (0.017 (μmol m-2 s-1) (μmol mol-1)-1) obtained in plants irrigated with water of 4.0 dS m-1 and under SA concentration of 3.6 mM.

The reductions in CEi are related to decreases in CO2 assimilation rate (Figure 4C) and increase in Ci (Figure 3), due to the low efficiency of the RuBisCO enzyme in CO2 carboxylation (Sousa et al., 2016SOUSA, J. R. M. et al. Impact of saline conditions and nitrogen fertilization on citrus production and gas exchanges. Revista Caatinga , 29(2):415-424, 2016.). It clearly indicates that salinity may have increased mesophilic resistance to the entry of atmospheric CO2 into carboxylation sites and/or reduced enzymatic activity associated with photosynthetic carbon metabolism, this effect being common in plants grown under saline conditions (Soares et al., 2021SOARES, L. A. A. et al. Physiological changes of pomegranate seedlings under salt stress and nitrogen fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental , 25(7):453-459, 2021.).

Salicylic acid concentrations significantly influenced the instantaneous water use efficiency of soursop (Figure 5). It is observed that plants subjected to SA concentration of 1.32 mM stood out with higher WUEi [3.47 (μmol m-2 s-1)(μmol mol-1)-1], with a reduction in WUEi when sprayed with SA concentrations above 1.32 mM. An increase of 6.6% [0.21 (μmol m-2 s-1) (μmol mol-1)-1] was found when comparing the WUEi of plants subjected to SA concentration of 1.32 mM to that of plants treated with SA concentration of 0 mM.

Salicylic acid caused increments in RWC (Figure 1B) and WUEi (Figure 5), and mitigated the effects of salt stress on the percentage of intercellular electrolyte leakage (Figure 2C). Plants sprayed with SA at concentrations between 1.2 and 1.6 mM and subjected to salt stress showed higher values of gs, E, A and CEi (Figures 4) compared to those cultivated without application of SA.

Figure 5:
Instantaneous water use efficiency - WUEi of soursop cv. Morada Nova as a function of salicylic acid concentrations - SA, at 480 days after transplanting. *, ** Significant at p ≤ 0.05 and p ≤ 0.01, respectively. The point and vertical lines represent Mean +/- Standard Error (n=3).

There was a significant effect of the interaction between salinity levels and SA concentrations on all growth variables, except on crown diameter (Table 4). Stem diameter, crown height, crown volume and vegetative vigor index were significantly (p<0.01) affected by salinity levels. On the other hand, salicylic acid concentrations significantly affected only crown height and volume. Besides this, the effect of block was significant on stem diameter and vegetative vigor index due to the reasons explained earlier.

Table 4:
Summary of the analysis of variance for stem diameter (SD), crown height (HCrown), crown diameter (DCrown), crown volume (VCrown) and vegetative vigor index (VVI) of soursop irrigated with saline water and under foliar application of salicylic acid, at 480 days after transplanting.

Spraying with SA up to a concentration of 1.6 mM promoted an increase in SD, HCrown, VCrown and VVI of soursop, regardless of the electrical conductivity of irrigation water (Figure 6A, 6B, 6C and 6D). It was observed that plants subjected to SA concentration of 1.6 mM and irrigated with water of 1.7 dS m-1 obtained higher values of SD (36.54 mm), HCrown (1.89 m), VCrown (1.25 m3) and VVI (3.19). When comparing in relative terms the SD, HCrown, VCrown and VVI of plants irrigated with water of 1.7 dS m-1 and subjected to SA concentration of 1.6 mM to the values of plants cultivated with the same salinity level (1.7 dS m-1), but without the application of SA (0 mM), there were increments of respectively, 4.84% (1.69 mm), 4.98% (0.09 m), 9.81% (0.11 m3) and 7.27% (0.55).

Figure 6:
Response surface for stem diameter (A), crown height (B), crown volume (C) and vegetative vigor index (D) of soursop cv. Morada Nova as a function of the interaction between the electrical conductivity of irrigation water - ECw and the concentrations of salicylic acid, at 480 days after transplanting. X and Y - ECw and salicylic acid concentration, respectively; *, ** Significant at p ≤ 0.05 and p ≤ 0.01 by F test.

Nowadays, soil and water salinity are continuously increasing due to climate change, global warming and human activities including intensive cultivation and application of chemical fertilizers (Hatamian et al., 2019HATAMIAN, M. et al. Growth characteristics of ornamental Judas tree (Cercis siliquastrum L.) seedling under different concentrations of lead and cadmium in irrigation water. Acta Scientiarum Polonorum Hortorum Cultus , 18(2):87-96, 2019.; Souri; Bakhtiarizade, 2019SOURI, M. K.; BAKHTIARIZADE, M. Biostimulation effects of Rosemary essential oil on growth and nutrient uptake of tomato seedlings. Scientia Horticulture, 243:472-476, 2019.). Different organic and inorganic compounds have shown to reduce the adverse effects of environmental constrains such as salinity (Souri; Hatamian, 2019SOURI, M. K.; HATAMIAN, M. Aminochelates in plant nutrition: A review. Journal of Plant Nutrition, 42(1):67-78, 2019.; Ahmadi; Souri, 2018AHMADI, M.; SOURI, M. K. Growth and mineral elements of coriander (Corianderum sativum L.) plants under mild salinity with different salts. Acta Physiologia Plantarum, 40(1):94-99, 2018.). In this context, salicylic acid plays an important role in the regulation of various physiological processes and plant development, besides increasing root cell growth through the division and expansion of the meristem, thus contributing to plant growth and development (Boukraâ et al., 2013BOUKRAÂ, D. et al. Effect of salinity on chickpea seed germination pre-treated with salicylic acid. Scientific Journal of Biological Sciences, 2(4):86-93, 2013.; Souri; Tohidloo, 2019SOURI, M. K.; TOHIDLOO, G. Effectiveness of different methods of salicylic acid application on growth characteristics of tomato seedlings under salinity. Chemical and Biological Technologies in Agriculture , 6:26, 2019.). Moreover, the beneficial effect of SA on gas exchange variables results improvement in growth parameters, as observed in the present study.

CONCLUSIONS

Foliar application of salicylic acid at concentrations between 1.2 and 1.6 mM mitigates the effects of salt stress on stomatal conductance, CO2 assimilation rate, transpiration and instantaneous carboxylation efficiency of soursop, at 480 days after transplanting. Spraying with salicylic acid at concentrations between 1.3 and 1.6 mM induces acclimatization of soursop plants to salt stress, since the percentage of intercellular electrolyte leakage was reduced and the growth was favored by the application of salicylic acid, even when exposed to salinity. Irrigation with water above 0.8 dS m-1 reduces the relative water content in the leaves of soursop cv. Morada Nova.

ACKNOWLEDGMENTS

To the National Council for Scientific and Technological Development - CNPq for granting financial aid (Proc. CNPq 430525/2018-4) and to the Coordination for the Improvement of Higher Education Personnel - CAPES for granting the scholarship to the first author.

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Publication Dates

  • Publication in this collection
    16 July 2021
  • Date of issue
    2021

History

  • Received
    02 Apr 2021
  • Accepted
    27 May 2021
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