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Methods of application of salicylic acid as attenuator of salt stress in cherry tomato

Métodos de aplicação de ácido salicílico como atenuantes do estresse salino em tomateiro cereja

Abstract

Salt stress caused by excess salts present in irrigation water, is one of the biggest barriers in agricultural production, especially in semi-arid regions. Thus, the use of substances, such as salicylic acid, that minimize the deleterious effects of salinity on plants can be an alternative to ensure satisfactory production. In this context, the objective of this study was to evaluate the effects of different methods of application of salicylic acid on the growth, production and water use efficiency of cherry tomato plants under salt stress. The study was conducted in a greenhouse, using an Entisol soil with a sandy loam texture. The treatments were distributed in a completely randomized design, in a 2×4 factorial arrangement, corresponding to two levels of electrical conductivity of irrigation water - ECw (0.6 and 2.6 dS m-1) and four methods of application of salicylic acid (Control - without application of SA; via spraying; via irrigation and via spraying and irrigation), with five replicates and one plant per plot. The salicylic acid concentration used in the different methods was 1.0 mM. Application of salicylic acid via foliar spraying increased the growth, production and water use efficiency of cherry tomato plants. The salt stress induced by the electrical conductivity of 2.6 dS m-1 was attenuated by the foliar application of salicylic acid. The use of water of 2.6 dS m-1 associated with the application of salicylic acid via irrigation water further intensified the adverse effects of salinity on cherry tomato plants.

Keywords:
Solanum lycopersicum L.; abiotic stress; brackish water; phytohormone

Resumo

O estresse salino ocasionado pelo excesso de sais presentes na água de irrigação, é um dos maiores entraves para a produção agrícola, sobretudo em regiões semiáridas. Assim, a utilização de substâncias, como o ácido salicílico, que minimizem os efeitos deletérios da salinidade sobre as plantas pode ser uma alternativa para garantir uma produção satisfatória. Neste contexto, objetivou-se com este trabalho avaliar os efeitos de diferentes métodos de aplicação de ácido salicílico sobre o crescimento, a produção e a eficiência do uso da água de plantas de tomate cereja sob estresse salino. O estudo foi conduzido em casa de vegetação, utilizando-se de um solo Entisol de textura franco-arenosa. Os tratamentos foram distribuídos em delineamento inteiramente casualizados, em arranjo fatorial 2×4, sendo duas condutividades elétricas da água de irrigação - CEa (0,6 e 2,6 dS m-1) e quatro métodos de aplicação de ácido salicílico (Testemunha - sem aplicação de AS; via pulverização; via irrigação e pulverização e irrigação), com cinco repetições e uma planta por parcela. A concentração de ácido salicílico utilizada nos diferentes métodos foi de 1,0 mM. A aplicação de ácido salicílico via pulverização foliar, aumentou o crescimento, a produção de plantas de tomate cereja, e a eficiência do uso da água. O estresse salino induzido pela condutividade elétrica de 2,6 dS m-1 foi amenizado pela aplicação foliar de ácido salicílico. O uso de água de 2,6 dS m-1 associado a aplicação de ácido salicílico via lâmina de irrigação, intensificou os efeitos adversos da salinidade nas plantas de tomate cereja.

Palavras-chave:
Solanum lycopersicum L.; estresse abiótico; águas salobras; fitormônio

1. Introduction

Tomato (Solanum lycopersicum L.) is among the main horticultural crops grown in a protected environment, especially cherry tomatoes, which is appreciated for having a strong aroma and unique flavor, it has 1.7 times the vitamin C content of conventional tomatoes, and helps in immunity, reducing blood pressure and cholesterol, besides preventing cancer (Liu et al., 2018LIU, H., MENG, F., MIAO, H., CHEN, S., YIN, T., HU, S., SHAO, Z., LIU, Y., GAO, L., ZHU, C., ZHANG, B. and WANG, Q., 2018. Effects of postharvest methyl jasmonate treatment on main health-promoting components and volatile organic compounds in cherry tomato fruits. Food Chemistry, vol. 263, no. 1, pp. 194-200. http://dx.doi.org/10.1016/j.foodchem.2018.04.124. PMid:29784307.
http://dx.doi.org/10.1016/j.foodchem.201...
; Zeng et al., 2020ZENG, C., TAN, P. and LIU, Z., 2020. Effect of exogenous ARA treatment for improving postharvest quality in cherry tomato (Solanum lycopersicum L.) fruits. Scientia Horticulturae, vol. 261, p. 108959. http://dx.doi.org/10.1016/j.scienta.2019.108959.
http://dx.doi.org/10.1016/j.scienta.2019...
). Cherry tomatoes also have a longer shelf time, around 18 days after harvest, making their commercialization more attractive (Matos et al., 2021MATOS, R.M., SILVA, P.F., DANTAS NETO, J., LIMA, A.S., LIMA, V.L.A. and SABOYA, L.M.F., 2021. Organic fertilization as an alternative to the chemical in cherry tomato growing under irrigation depths. Bioscience Journal, vol. 37, no. 1, e37006. http://dx.doi.org/10.14393/BJ-v37n0a2021-48270.
http://dx.doi.org/10.14393/BJ-v37n0a2021...
).

Irrigation water quality is one of the most important factors for plants to express their maximum production potential, especially in protected cultivation, since in this production system there is no leaching of salts by rainwater, as occurs naturally in areas cultivated in the open fields (Guedes et al., 2015GUEDES, R.A., OLIVEIRA, F.A., ALVES, R.C., MEDEIROS, A.S., GOMES, L.P. and COSTA, L.P., 2015. Estratégias de irrigação com água salina no tomateiro cereja em ambiente protegido. Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 19, no. 10, pp. 913-919. http://dx.doi.org/10.1590/1807-1929/agriambi.v19n10p913-919.
http://dx.doi.org/10.1590/1807-1929/agri...
; Roque et al., 2022ROQUE, I.A., SOARES, L.A.A., LIMA, G.S., LOPES, I.A.P., SILVA, L.A. and FERNANDES, P.D., 2022. Biomass, gas exchange and production of cherry tomato cultivated under saline water and nitrogen fertilization. Revista Caatinga, vol. 35, no. 3, pp. 686-696. http://dx.doi.org/10.1590/1983-21252022v35n320rc.
http://dx.doi.org/10.1590/1983-21252022v...
).

The semi-arid region of Northeast Brazil presents water restrictions in terms of quality and quantity, making the production of vegetable crops dependent on irrigation, which is often carried out with water that has a high salt content (Silva et al., 2024SILVA, A.A.R., CAPITULINO, J.D., LIMA, G.S., AZEVEDO, C.A.V., ARRUDA, T.F.L., SOUZA, A.R., GHEYI, H.R. and SOARES, L.A.A., 2024. Hydrogen peroxide in attenuation of salt stress effects on physiological indicators and growth of soursop. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e261211. http://dx.doi.org/10.1590/1519-6984.261211. PMid:35792744.
http://dx.doi.org/10.1590/1519-6984.2612...
). Irrigation with saline water can cause the accumulation of sodium (Na+) and chloride (Cl-) ions, and their excess restricts the absorption of water and nutrients by the roots of plants, compromising their growth and development (Hussain et al., 2021HUSSAIN, S., HUSSAIN, S., ALI, B., REN, X., CHEN, X., LI, Q., SAQIB, M. and AHMAD, N., 2021. Recent progress in understanding salinity tolerance in plants: story of Na+/K+ balance and beyond. Plant Physiology and Biochemistry, vol. 160, pp. 239-256. http://dx.doi.org/10.1016/j.plaphy.2021.01.029. PMid:33524921.
http://dx.doi.org/10.1016/j.plaphy.2021....
). Salt stress also causes several plant disorders, including reduction in stomatal conductance, inhibition of photosynthesis, reduction in protein synthesis, impairment of enzymatic activities and chlorophyll degradation (Liang et al., 2018LIANG, W., MA, X., WAN, P. and LIU, L., 2018. Plant salt-tolerance mechanism: a review. Biochemical and Biophysical Research Communications, vol. 495, no. 1, pp. 286-291. http://dx.doi.org/10.1016/j.bbrc.2017.11.043. PMid:29128358.
http://dx.doi.org/10.1016/j.bbrc.2017.11...
).

Salicylic acid (SA) is a plant hormone that plays several physiological roles in plants, including promoting growth, floral induction, nutrient absorption, ethylene biosynthesis, stomatal closure and photosynthesis (Silva et al., 2020SILVA, A.A.R., LIMA, G.S., AZEVEDO, C.A.V., VELOSO, L.L.S.A. and GHEYI, H.R., 2020. Salicylic acid as an attenuator of salt stress in soursop. Revista Caatinga, vol. 33, no. 4, pp. 1092-1101. http://dx.doi.org/10.1590/1983-21252020v33n424rc.
http://dx.doi.org/10.1590/1983-21252020v...
). The SA activates the plant’s defense response by inducing tolerance to abiotic stresses, such as salt stress, by improving physiological processes, accelerating plant growth and reducing oxidative damage (Jayakannan et al., 2015JAYAKANNAN, M., BOSE, J., BABOURINA, O., RENGEL, Z. and SHABALA, S., 2015. Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regulation, vol. 76, no. 1, pp. 25-40. http://dx.doi.org/10.1007/s10725-015-0028-z.
http://dx.doi.org/10.1007/s10725-015-002...
; Oliveira et al., 2022OLIVEIRA, V.K.N., LIMA, G.S., SOARES, M.D.M., SOARES, L.A.A., GHEYI, H.R., SILVA, A.A.R., PAIVA, F.J.S., MENDONÇA, A.J.T. and FERNANDES, P.D., 2022. Salicylic acid does not mitigate salt stress on the morphophysiology and production of hydroponic melon. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, e262664. PMid:36197402.).

In recent years, studies have reported that the application of salicylic acid can attenuate the effects of salt stress in several vegetables, for example, Veloso et al. (2021)VELOSO, L.L.S.A., LIMA, G.S., SILVA, A.A.R., SOUZA, L.P., LACERDA, C.N., SILVA, I.J., CHAVES, L.H.G. and FERNANDES, P.D., 2021. Attenuation of salt stress on the physiology and production of bell peppers by treatment with salicylic acid. Semina: Ciências Agrárias, vol. 42, no. 5, pp. 2751-2768. http://dx.doi.org/10.5433/1679-0359.2021v42n5p2751.
http://dx.doi.org/10.5433/1679-0359.2021...
found that foliar application of SA at a concentration of 1.6 mM increased chlorophyll biosynthesis, and the number of sweet pepper fruits; Sousa et al. (2024)SOUSA, V.F.O., SANTOS, A.S., SALES, W.S., SILVA, A.J., GOMES, F.A.L., DIAS, T.J., GONÇALVES-NETO, A.C., FARAZ, A., SANTOS, J.P.O., SANTOS, G.L., CRUZ, J.M.F.L., SILVA, L.D.R. and ARAÚJO, J.R.E.S., 2024. Exogenous application of salicylic acid induces salinity tolerance in eggplant seedlings. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e257739. http://dx.doi.org/10.1590/1519-6984.257739. PMid:35081218.
http://dx.doi.org/10.1590/1519-6984.2577...
observed that foliar application of SA at a concentration of 1 mM reduced cell membrane damage and increased the relative water content of eggplant leaves. In basil, Silva et al. (2022)SILVA, T.I.D., SILVA, J.D.S., DIAS, M.G., MARTINS, J.V.D.S., RIBEIRO, W.S. and DIAS, T.J., 2022. Salicylic acid attenuates the harmful effects of salt stress on basil. Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 26, no. 6, pp. 399-406. http://dx.doi.org/10.1590/1807-1929/agriambi.v26n6p399-406.
http://dx.doi.org/10.1590/1807-1929/agri...
found improvements in gas exchange as a function of the application of SA (1 mM). However, these studies are limited to application of salicylic acid through a single method.

The beneficial effect of SA application depends on the plant species, stage of development, outype of cultivation, concentration applied and the method of application used (Ferrareze et al., 2019FERRAREZE, J.P., CASTILHO, M.S.M., SGANZERLA, W.G. and PIOVEZAN, M., 2019. Toxicity of salicylic acid and acetylsalicylic acid in Raphanus sativus submitted to water stress. Acta Horticulturae, vol. 1251, pp. 159-164. http://dx.doi.org/10.17660/ActaHortic.2019.1251.23.
http://dx.doi.org/10.17660/ActaHortic.20...
). In this context, the objective of this study was to evaluate the effects of the methods of SA application on the growth, production and water use efficiency of cherry tomato plants under salt stress, in a protected environment.

2. Material and Methods

2.1. Localization and treatments

The experiment was carried out between October 2020 and February 2021, in a greenhouse, belonging to the Academic Unit of Agricultural Engineering - UAEA of the Federal University of Campina Grande - UFCG, in Campina Grande, Paraíba, Brazil, located at the geographical coordinates 7°15’18” South latitude, 35°52’28” West longitude and mean altitude of 550 m. The greenhouse used is of the arched type, 22 m long and 6.5 m wide, with a ceiling height of 3.0 m and a low density infrared treated polyethylene cover (150 microns). The data of temperature (maximum and minimum) and average relative air humidity of the experimental site 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 resulted from the combination of two levels of electrical conductivity of irrigation water - ECw (S1= 0.6 dS m-1 and S2= 2.6 dS m-1) and four methods of application of salicylic acid - MA (M1= Control - without application of SA, M2= via spraying, M3= via irrigation and M4=via spraying and irrigation), in a 2×4 factorial arrangement (Table 1), distributed in a completely randomized design, with five replicates each consisting of one plant.

Table 1
Description of the analyzed treatments.

The SA concentration used in the different application methods was same (1.0 mM), based on studies conducted by Jahan et al. (2019)JAHAN, M.S., WANG, Y., SHU, S., ZHONG, M., CHEN, Z., WU, J., SU, J., and GUO, S., 2019. Exogenous salicylic acid increases the heat tolerance in tomato (Solanum lycopersicum L.) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Scientia Horticulturae, vol. 247, no. 1, pp. 421-429. http://dx.doi.org/10.1016/j.scienta.2018.12.047.
http://dx.doi.org/10.1016/j.scienta.2018...
and Poursakhi et al. (2019)POURSAKHI, N., RAZMJOO, J. and KARIMMOJENI, H., 2019. Interactive effect of salinity stress and foliar application of salicylic acid on some physiochemical traits of chicory (Cichorium intybus L.) genotypes. Scientia Horticulturae, vol. 258, no. 1, p. 108810. http://dx.doi.org/10.1016/j.scienta.2019.108810.
http://dx.doi.org/10.1016/j.scienta.2019...
with tomato crop. The levels of electrical conductivity of irrigation water (0.6 and 2.6 dS m-1) were selected in accordance with the results of a study reported by Vieira et al. (2016)VIEIRA, I.G.S., NOBRE, R.G., DIAS, A.S. and PINHEIRO, F.W.A., 2016. Cultivation of cherry tomato under irrigation with saline water and nitrogen fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 20, no. 1, pp. 55-61. http://dx.doi.org/10.1590/1807-1929/agriambi.v20n1p55-61.
http://dx.doi.org/10.1590/1807-1929/agri...
on cherry tomatoes keeping in view salt tolerance of crop).

2.2. Plant material

The cherry tomato cultivar used was ‘Carolina’, which has indeterminate growth, fruits with red color and small size, weighing from 10 to 12 g, and a cycle of 110 to 120 days, being resistant to verticillium wilt (Verticillium albo-atrum and Verticillium dahliae) and fusarium (Fusarium oxysporum). The fruit has longer shelf life, around 18 days after harvest (Matos et al., 2021MATOS, R.M., SILVA, P.F., DANTAS NETO, J., LIMA, A.S., LIMA, V.L.A. and SABOYA, L.M.F., 2021. Organic fertilization as an alternative to the chemical in cherry tomato growing under irrigation depths. Bioscience Journal, vol. 37, no. 1, e37006. http://dx.doi.org/10.14393/BJ-v37n0a2021-48270.
http://dx.doi.org/10.14393/BJ-v37n0a2021...
).

2.3. Establishment and management of the experiment

The experiment was conducted using Citropote® pots of 8 dm3 volume and 4 dm2 area, covered with a geotextile (Bidim OP 30) and filled with a 0.3-kg layer of crushed stone (n° = 0) followed by 8 kg of soil classified as Entisol (USDA, 2014UNITED STATES DEPARTMENT OF AGRICULTURE – USDA, 2014. Keys to soil taxonomy. Washinton: Natural Resources Conservation Service, 372 p.), collected at a depth of 0-30 cm, from the municipality of Riachão do Bacamarte-PB, whose physico-chemical attributes (Table 2) were determined according to Teixeira et al. (2017)TEIXEIRA, P.C., DONAGEMMA, G.K., FONTANA, A. and TEIXEIRA, W.G., 2017. Manual de métodos de análise de solo. 3ª ed. Brasília: Embrapa Solos, 574 p..

Table 2
Chemical and physical attributes of the soil (0-0.30 m layer), used in the experiment, before the application of the treatments. Campina Grande, PB.

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 = 0.32 dS m-1). This proportion is commonly found in sources of water used for irrigation in small properties in the Northeast (Medeiros et al., 2003MEDEIROS, J.F., LISBOA, R.A., OLIVEIRA, M., SILVA JÚNIOR, M.J. and ALVES, L.P., 2003. Caracterização das águas subterrâneas usadas para irrigação na área produtora de melão da Chapada do Apodi. Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 7, no. 3, pp. 469-472. http://dx.doi.org/10.1590/S1415-43662003000300010.
http://dx.doi.org/10.1590/S1415-43662003...
). The irrigation waters were prepared considering the relationship between ECw and concentration of salts, according to Richards (1954)RICHARDS, L.A., 1954. Diagnosis and improvement of saline and alkali soils. Washington: U.S. Department of Agriculture, 160 p., as shown in Equation 1:

C 10 × ECw (1)

where: C - concentration of salts (mmolc L-1); ECw - electrical conductivity of water (dS m-1).

Sowing was carried out by placing three tomato seeds at 2 cm depth, distributed equidistantly, in 250-mL disposable plastic cups; at 10 days after sowing (DAS), thinning was performed in order to leave only one plant per cup with the greatest vigor. Transplanting to Citropote® pot was performed at 20 days after sowing.

At 30 DAS, irrigation with saline waters began to be applied, adopting a two-day irrigation interval, applying adequate volume of water to maintain soil moisture close to field capacity. The volume to be applied was determined according to the water requirement of the plants, estimated by the water balance, as shown in Equation 2:

VI = Va Vd 1 LF (2)

where: VI - volume of water to be applied in irrigation (mL); Va - volume applied in the previous event of irrigation (mL);

Vd - volume drained after previous event of irrigation (mL); LF - leaching fraction of 0.15, applied every 20 days.

The concentration of salicylic acid (SA) was obtained by dissolution of product in ethyl alcohol (30%), since it is a substance with low solubility in water at room temperature, and the pH of salicylic acid after the preparation of the 1.0 mM concentration was 2.2. To reduce the surface tension of the drops on the leaf surface, the adjuvant Wil fix at the concentration of 0.5 mL L-1 was used in the preparation of the solution.

The applications of SA began five days before irrigation with saline water, that is, at 25 DAS, spraying the abaxial and adaxial sides of the leaves. Subsequent applications were performed at intervals of 15 days, up to 85 DAS, using a sprayer between 17:00 and 17:30 hours, with an average volume of 150 mL applied per plant in each spraying. Plants subjected to the method of application via irrigation were irrigated with a volume of 50 mL of SA on the same days of the spraying and in application by irrigation and spraying same doses and procedres were used.

Fertilization with nitrogen, potassium and phosphorus was performed through top-dressing, using doses recommended by Novais et al. (1991)NOVAIS, R.F., NEVES, J.C.L. and BARROS, N.F., 1991. Ensaio em ambiente controlado. In: A.J. OLIVEIRA, ed. Métodos de pesquisa em fertilidade do solo. Brasília: Embrapa-SEA, pp. 189-253.. 0.76 g of urea, 2.0 g of potassium chloride and 3.87 g of monoammonium phosphate, equivalent to 100, 150 and 300 mg kg-1 of N, K2O and P2O5, respectively, were applied in four equal applications via fertigation, at intervals of 15 days, with the first application being performed at 40 days after sowing (DAS).

A micronutrient solution was applied fortnightly at the concentration of 1.0 g L-1 of the commercial product Dripsol® micro containing: Mg (1.1%); Zn (4.2%); B (0.85%); Fe (3.4%); Mn (3.2%); Cu (0.5%); Mo (0.05%), on the leaves, covering their adaxial and abaxial sides, using a backpack sprayer.

During the experiment, all cultural practices and phytosanitary treatments recommended for the crop were carried out, monitoring the emergence of pests and diseases and adopting appropriate control measures when necessary.

2.4. Traits measured

Growth was evaluated based on plant height (PH), stem diameter (SD), relative growth rates in plant height (RGRPH) and stem diameter (RGRSD); production variables: number of fruits per plant (NF), averagemean fruit weight (mFW), total production per plant (TPP), polar (PD) and equatorial diameter (ED) of the fruit; water consumption (WC) and water use efficiency (WUE).

Growth was measured at 80 (PH1 and SD1) and 110 DAS (PH2 and SD2). Plant height was measured using as reference the distance from the plant collar to the apical meristem, and stem diameter (mm) was measured two centimeters above the plant collar. The data of PH (PH1 and PH2) and SD (SD1 and SD2) were used to determine the relative growth rate, a variable that indicates the growth rate of the plants when the final height/diameter is compared with the initial one. The relative growth rate was determined according to the methodology described by Benincasa (2003)BENINCASA, M.M.P., 2003. Análise de crescimento de plantas: noções básicas. 2ª ed. Jaboticabal: FUNEP, 41 p..

Ripe fruits were harvested from 90 DAS, extending up to 120 DAS, when the number of fruits per plant was counted and the mean fruit weight as well as total production per plant were determined. PD and ED were obtained with a digital caliper. Water consumption by the plants was obtained by summing up the water volume applied throughout the crop cycle (120 days), subtracting the sum of the drained water volume. Water use efficiency (kg m-3) was determined by the ratio of total production per plant (kg) and water consumption (m3) per plant, according to Guan et al. (2015)GUAN, D., ZHANG, Y., AL-KAISI, M.M., WANG, Q., ZHANG, M. and LI, Z., 2015. Tillage practices effect on root distribution and water use efficiency of winter wheat under rain-fed condition in the North China Plain. Soil & Tillage Research, vol. 146, no. 1, pp. 286-295. http://dx.doi.org/10.1016/j.still.2014.09.016.
http://dx.doi.org/10.1016/j.still.2014.0...
.

2.5. Statistical analysis

The multivariate structure of the results was evaluated by means of principal component analysis (PCA), synthesizing the amount of relevant information contained in the original data set in a smaller number of dimensions, resulting from linear combinations of the original variables generated from the eigenvalues (λ ≥ 1.0) in the correlation matrix, explaining a percentage greater than 10% of the total variance (Govaerts et al., 2007GOVAERTS, B., SAYRE, K.D., LICHTER, K., DENDOOVEN, L. and DECKERS, J., 2007. Influence of permanent raised bed planting and residue management on physical and chemical soil quality in rain fed maize/wheat systems. Plant and Soil, vol. 291, no. 1-2, pp. 39-54. http://dx.doi.org/10.1007/s11104-006-9172-6.
http://dx.doi.org/10.1007/s11104-006-917...
).

From the reduction of dimensions, the original data of the variables of each component were subjected to multivariate analysis of variance (MANOVA) by the Hotelling test (Hotelling et al., 1947HOTELLING, H., EISENHART, C., HASTAY, M.W. and WALLIS, W.A., 1947. Multivariate quality control. Techniques of statistical analysis. New York: John Wiley & Sons.) at 0.05 probability level for the electrical conductivity of irrigation water and the methods of salicylic acid application, as well as for the interaction between them.

Only variables with correlation coefficient greater than or equal to 0.6 were maintained in each principal component (PC) (Hair et al., 2009HAIR, F.J., BLACK, W.C., BABIN, B.J., ANDERSON, R.E. and TATHAM, R.L., 2009. Análise multivariada de dados. 6th ed. Porto Alegre. The Bookman, 688 p.). Statistical analyses were performed using the software program Statistica v. 7.0 (Statsoft, 2004STATSOFT, 2004. Statistica: data analysis software system. Version 7. Tulsa: Statsoft Inc..).

3. Results and Discussion

The multidimensional space of the original variables was reduced to two principal components (PC1 and PC2) with eigenvalues greater than λ ≥ 1.0, according to Kaiser (1960)KAISER, H.F., 1960. The application of electronic computers to factor analysis. Educational and Psychological Measurement, vol. 20, no. 1, pp. 141-151. http://dx.doi.org/10.1177/001316446002000116.
http://dx.doi.org/10.1177/00131644600200...
. The eigenvalues and percentage of variation explained for each component (Table 3) together represent 87.9% of the total variation. PC1 explained 71.61% of the total variance, formed by most of the variables analyzed, except for the relative growth rates. PC2 represented 16.25% of the remaining variance, being formed by the variables RGRPH, RGRSD and WC.

Table 3
Eigenvalues, percentage of total variance explained in the multivariate analysis of variance (MANOVA) and coefficient of correlations (r) between original variables and the principal components.

According to the multivariate analysis of variance (Table 3), there was a significant effect of the interaction between salinity levels (NS) and the methods of application of salicylic acid (MA). Salinity levels also influenced the two PCs. On the other hand, the methods of application of SA caused significant effect (p ≤ 0.01) only on PC1.

The two-dimensional projections of the effects of treatments and variables in the first and second principal component (PC1 and PC2) are shown in Figures 2A and 2B. In the first principal component (PC1), a process possibly characterized by the effect of the interaction between irrigation water salinity and the methods of application of salicylic acid was identified, and it is also verified that the correlation coefficients between PH1, PH2, SD1, SD2, NF, MFW, TPP, PD, ED and WUE were higher than 0.70.

Figure 2
Two-dimensional projection of the scores of the principal components for the factors salinity levels (S) and methods of application of salicylic acid (M) (A) and the variables analyzed (B) in the first two principal components (PC1 and PC2).

In the principal component 1, it is possible to observe that cherry tomato plants irrigated with water of 0.6 dS m-1 and cultivated with foliar spraying of salicylic acid (treatment S1M2) stood out from those of the other treatments, considering that the highest values (Table 3) of PH2 (89.6 cm), SD2 (13.0 mm), NF (37), MFW (3.3 g), TPP (114.5 g per plant), PD (20.4 mm), ED (16.6 mm) and WUE (4.6 kg m-3) were obtained. Plants irrigated with water of 2.6 dS m-1 and subjected to SA application via spraying (treatment S2M2) obtained the highest growth in PH1 (67 cm) and SD1 (11.1 mm).

When comparing the results obtained in plants of the S1M2 treatment to those of plants of the S1M1 treatment, there were increments of 3.94, 7.44, 42.31, 6.45, 45.67, 3.03, 4.40 and 43.75% in PH2, SD2, NF, MFW, TPP, PD, ED and WUE, respectively, demonstrating beneficial effect of salicylic acid spraying on the growth and production of cherry tomato plants.

Also in the principal component 1, it is verified that the lowest values of PH1 (55 cm), PH2 (70.60 cm), SD1 (8.1 mm), SD2 (9.9 mm), NF (10), MFW (2.2 g), TPP (30 g per plant), PD (17.7 mm), ED (14.3 mm) and WUE (1.6 kg m-3) were found in the treatment S2M3, thus highlighting that the SA application via irrigation depth intensifies the deleterious effects of salt stress.

When analyzing the principal component 2 (PC2), it can be verified that the relative growth rates in plant height and stem diameter and water consumption are the most important variables for the second principal component, due to the higher values of correlation observed (Table 3). Cherry tomato plants irrigated with water of 0.6 dS m-1 and subjected to spraying and irrigation with salicylic acid simultaneously obtained the highest value of RGRPH (0.0125 cm cm d-1), RGRSD (0.0088 mm mm d-1) and WC (619.8 mm).

It is possible to observe in this study that spraying with salicylic acid also mitigated the deleterious effects of irrigation water salinity on the growth and production of cherry tomatoes (Table 3), and plants irrigated with water of 2.6 dS m-1 and sprayed with SA (S2M4) showed increments of 13.6, 15.8, 14.4, 16.0, 66.7, 10.7, 89.7, 4.8, 6.5 and 66.7% in PH1, PH2, SD1, SD2, NF, MFW, TPP, PD, ED and WUE, respectively, compared to plants irrigated with the same salinity level and without application of SA (S2M1).

Salt stress is one of the main factors that reduce plant growth and yield. In this study, it was verified that growth and production compromised in plants exposed to salt stress. At high concentrations, water and/or soil salinity affects the absorption of water and nutrients and all physiological processes of plants (Kamanga and Mndala, 2019KAMANGA, R.M. and MNDALA, L., 2019. Crop abiotic stresses and nutrition of harvested food crops: a review of impacts, interventions and their effectiveness. African Journal of Agricultural Research, vol. 14, no. 3, pp. 118-135. http://dx.doi.org/10.5897/AJAR2018.13668.
http://dx.doi.org/10.5897/AJAR2018.13668...
).

According to Assaha et al. (2017)ASSAHA, D.V.M., MEKAWY, A.M.M., LIU, L., NOORI, M.S., KOKULAN, K.S., UEDA, A., NAGAOKA, T. and SANEOKA, H., 2017. Na+ retention in the root is a key adaptive mechanism to low and high salinity in the glycophyte, Talinum paniculatum (Jacq.) Gaertn. (Portulacaceae). Journal Agronomy & Crop Science, vol. 203, no. 1, pp. 56-67. http://dx.doi.org/10.1111/jac.12184.
http://dx.doi.org/10.1111/jac.12184...
, Na+ and K+ ions compete for the same binding sites due to their similar physical-chemical properties, so that excess Na+ in the growth medium results in the substitution of K+ in some biochemical reactions, which can inhibit enzymatic functions and compromise membrane integrity. In addition, salt stress induces excessive generation of reactive oxygen species (ROS) (Abdelaziz et al., 2018ABDELAZIZ, M.N., XUAN, T.D., MEKAWY, A.M.M., WANG, H. and KHANH, T.D., 2018. Relationship of salinity tolerance to Na+ exclusion, proline accumulation, and antioxidant enzyme activity in rice seedlings. Agriculture, vol. 8, no. 11, pp. 166-178. http://dx.doi.org/10.3390/agriculture8110166.
http://dx.doi.org/10.3390/agriculture811...
). Vieira et al. (2016)VIEIRA, I.G.S., NOBRE, R.G., DIAS, A.S. and PINHEIRO, F.W.A., 2016. Cultivation of cherry tomato under irrigation with saline water and nitrogen fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 20, no. 1, pp. 55-61. http://dx.doi.org/10.1590/1807-1929/agriambi.v20n1p55-61.
http://dx.doi.org/10.1590/1807-1929/agri...
, in a study with cherry tomatoes under saline stress (0.3 to 4.5 dS m-1), observed reductions of 27.4% (45.52 cm) in plant height and 21.3% (2.96 mm) in stem diameter in plants irrigated with water with higher electrical conductivity. Naeem et al. (2020)NAEEM, M., BASIT, A., AHMAD, I., MOHAMED, H.I. and WASILA, H., 2020. Effect of salicylic acid and salinity stress on the performance of tomato plants. Gesunde Pflanzen, vol. 72, no. 4, pp. 393-402. http://dx.doi.org/10.1007/s10343-020-00521-7.
http://dx.doi.org/10.1007/s10343-020-005...
evaluated the cherry tomato crop under salt stress (0 to 90 mM) and found a 71,6% reduction in production variables when plants were exposed to higher salinity levels.

Despite the deleterious effect of salinity on cherry tomato plants, it was verified in the present study that the application of salicylic acid by foliar spraying favored their growth, production and water use efficiency. Spraying of SA was able to mitigate the negative effects caused by salt stress on the variables: PH1, PH2, SD1, SD2, NF, MFW, TPP, PD, ED and WUE.

Yildirim and Dursun (2009)YILDIRIM, E. and DURSUN, A., 2009. Effect of foliar salicylic acid applications on plant growth and yield of tomato under greenhouse conditions. Acta Horticulturae, vol. 807, pp. 395-400. http://dx.doi.org/10.17660/ActaHortic.2009.807.56.
http://dx.doi.org/10.17660/ActaHortic.20...
observed higher growth and yield and better quality of tomato in response to foliar application of SA under greenhouse conditions. Souri and Tohidloo (2019)SOURI, M.K. and TOHIDLOO, G., 2019. Effectiveness of different methods of salicylic acid application on growth characteristics of tomato seedlings under salinity. Chemical and Biological Technologies in Agriculture, vol. 6, no. 1, p. 26. http://dx.doi.org/10.1186/s40538-019-0169-9.
http://dx.doi.org/10.1186/s40538-019-016...
, in a study evaluating the efficacy of different methods of salicylic acid application in the growth characteristics of tomato under salt stress, verified that foliar application of SA promoted increased growth in plant height and leaf area, and foliar spraying with SA also reduced the concentration of Na+ in leaves.

The positive effects of salicylic acid on the mitigation of salt stress can be attributed to higher absorption of water and nutrients, membrane protection and increased photosynthetic activity, as it can also interact with signaling pathways of ROS and reduce oxidative stress (Saleem et al., 2021SALEEM, M., FARIDUDDIN, Q. and CASTROVERDE, C.D.M., 2021. Salicylic acid: a key regulator of redox signalling and plant immunity. Plant Physiology and Biochemistry, vol. 168, no. 1, pp. 381-397. http://dx.doi.org/10.1016/j.plaphy.2021.10.011. PMid:34715564.
http://dx.doi.org/10.1016/j.plaphy.2021....
).

Salicylic acid also acts by regulating physiological and biochemical processes in plants, preventing the reduction of auxin and cytokinin levels, leading to a better cell division of the root apical meristem, thus promoting plant growth and yield (Osama et al., 2019OSAMA, S., SHEREI, M., AL-MAHDY, D.A., BISHR, M. and SALAMA, O., 2019. Effect of salicylic acid foliar spraying on growth parameters, γ-pyrones, phenolic content and radical scavenging activity of drought stressed Ammi visnaga L. plant. Industrial Crops and Products, vol. 134, no. 1, pp. 1-10. http://dx.doi.org/10.1016/j.indcrop.2019.03.035.
http://dx.doi.org/10.1016/j.indcrop.2019...
).

The increase in growth variables as a function of foliar application of salicylic acid also resulted in higher production of cherry tomato fruits and, consequently, in the increase of water use efficiency. Salicylic acid optimizes nutrient absorption by plants and increases photosynthetic activity and biochemical processes, directly contributing to plant growth and development under salt stress (Tahjib-Ul-Arif et al., 2018TAHJIB-UL-ARIF, SIDDIQUI, N., SOHAG, A.A.M., SAKIL, A., RAHMAN, M., POLASH, M.A.S., MOSTAFA, M.G. and TRAN, L.-S.P., 2018. Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. Journal of Plant Growth Regulation, vol. 37, no. 4, pp. 1318-1330. http://dx.doi.org/10.1007/s00344-018-9867-y.
http://dx.doi.org/10.1007/s00344-018-986...
; Oliveira et al., 2022OLIVEIRA, V.K.N., LIMA, G.S., SOARES, M.D.M., SOARES, L.A.A., GHEYI, H.R., SILVA, A.A.R., PAIVA, F.J.S., MENDONÇA, A.J.T. and FERNANDES, P.D., 2022. Salicylic acid does not mitigate salt stress on the morphophysiology and production of hydroponic melon. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, e262664. PMid:36197402.).

In this study, it was also found that the application of salicylic acid via irrigation depth was harmful to the cherry tomato crop, especially when irrigated with water of 2.6 dS m-1. This result may be related to the acidity (pH = 2.2) of the SA solution, which in direct contact with the root system may have compromised the development and, consecutively, the absorption of nutrients by plants.

In general, it can be inferred that the use of salicylic acid via foliar spraying can be an alternative to increase the yield of cherry tomatoes in a protected environment, also helping to reduce the harmful effects of salt stress.

4. Conclusions

Application of salicylic acid via foliar spraying increases the growth, production and water use efficiency of cherry tomato plants. The salt stress induced by the electrical conductivity of 2.6 dS m-1 is alleviated by the foliar application of salicylic acid. The use of water of 2.6 dS m-1, combined with salicylic acid application via irrigation depth, intensifies the harmful effects of salinity.

Acknowledgements

The authors gratefully acknowledge the Post-Graduate Agricultural Engineering Program at Universidade Federal de Campina Grande. To the National Council for Scientific Development and Technology (CNPq) for awarding a Post-Doctoral Junior fellowship to the first autor (Proc. 150927/2022-3) and Coordination of Improvement of Higher Education Personnel (CAPES).

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Publication Dates

  • Publication in this collection
    28 Oct 2022
  • Date of issue
    2022

History

  • Received
    18 June 2022
  • Accepted
    06 Oct 2022
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