Document Type : Original Article

Authors

1 Ph.D. student, Department of Horticultural Sciences, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

2 Professor, Department of Horticultural Sciences, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

3 Associate Professor, Department of Horticultural Sciences, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

10.22077/escs.2024.6547.2227

Abstract

Introduction
Physalis (Physalis peruviana L.) is a perennial plant belonging to the Solanaceae family, but it is grown commercially as an annual crop. Low temperature has been reported as one of the most restraining environmental factors for agricultural crops, particularly vegetables. Cold stress causes symptoms such as wilting, reduced growth and photosynthetic rate, chlorosis, necrosis, discoloration, abnormal ripening, increased susceptibility to diseases, ion leakage from cell membranes, and changes in respiration and ethylene production in plants. Amino acids are one of the possible approaches that induce cold stress tolerance in plants. Phenylalanine is one of the essential amino acids that is used as a nutritional enhancer, amino acid injection, and complex amino acid preparation. Foliar application of amino acids such as L-phenylalanine during plant growth increased anthocyanins and phenolic compounds contents in grape and strawberry fruits and cysteine also contains sulfur as an amino acid which is widely present in bacteria, yeast, plants, animals and certain single cells. Spraying amino acids on plants is one of the modern methods. Selenium (Se) and its salts protect plants against biotic (pathogens and herbivores) and abiotic (ultraviolet rays, heavy metals, arsenic) stresses. Also, the findings showed that selenium can effectively stimulate the phenylpropanoid metabolic pathway and it has been specifically determined that it protects plants against biological stresses.
Materials and methods
In order to investigate the effect of low temperature stress during seedling growth stage, and foliar application of amino acids L-phenylalanine (Phe), L-cysteine (Cys) and sodium selenite (Se) on yield and fruit quality of Physalis (Physalis peruviana L.), an experiment was conducted in greenhouse and field of University of Zanjan. The seeds of physalis were sown in seedling trays contain peat moss. The seedlings were grown under normal conditions (25±2 °C/day and 20±2 °C at night with 60-65% RH). The different concentrations of Phe (0.75, 1.5 and 2.5 mM), Cys (0.25, 0.5, and 0.75 mM) and Se (0.25, 0.5, and 1 mg.L-1) was sprayed on the seedling at 4–5th true leaf stage and distilled water was used for control treatment. For the chilling stress treatment of seedlings, plants were transferred to the 4 °C climate chamber for 24 h and two days. The control group (plants without chilling stress) was grown under normal conditions (25±2 °C/day and 20±2 °C at night with 60-65% RH). Plants transplanted to the field and foliar sprayed three times (growth stage, flowering and fruit set stages) with amino acids and Se. Fruits were harvested with the change of calyx and fruit color from green to orange and total fruit yield estimated as a kg.ha-1. Also, chlorophyll and carotenoid contents of leaf, fruit carotenoid, titratable acidity, soluble solids contents, vitamin C ant antioxidant activity were investigated.
Results and discussion
The results showed that low temperature significantly decreased total chlorophyll and carotenoid contents of leaves, titratable acidity (TA) and carotenoid contents of fruit, and caused increases in total soluble solid content of fruit, but had no significant difference on fruit yield, vitamin C content and antioxidant activity. Foliar application of Phe, Cys, and Se increased yield and fruit quality. The highest fruit yield (11419.1 kg.ha-1) was obtained in with application of Cys 0.5 mM in plants under low temperature stress. The maximum vitamin C content was obtained in plants sprayed with Phe 0.75 and 1.5 mM under normal condition. Also, the highest fruit antioxidant activity (56.9%) was observed with application of Phe 0.75 mM in plants without cold stress compared to other treatments and plants under stress. The beneficial role of Se and amino acids in increasing antioxidant capacity might be attributed to enhancing antioxidant enzymes activity, phenolic compounds and carotenoids content, which have antioxidant activity.
Conclusion
Therefore, the use of these compounds specially Phe 1.5 mM, Cys 0.5 mM and Se 1 mg.L-1 are suggested to improve the performance and quality of the fruit under low temperature stress or non-stress conditions.

Keywords

Main Subjects

Aghdam, M.S., Moradi, M., Razavi, F., Rabiei, V., 2019. Exogenous phenylalanine application promotes chilling tolerance in tomato fruits during cold storage by ensuring supply of NADPH for activation of ROS scavenging systems. Scientia Horticulturae. 246, 818-825. https://doi.org/10.1016/j.scienta.2018.11.074
Ali, S., Khan, A.S., Malik, A.U., 2016. Postharvest L-cysteine application delayed pericarp browning, suppressed lipid peroxidation and maintained antioxidative activities of litchi fruit. Postharvest Biology and Technology. 121, 135-142. https://doi.org/10.1016/j.postharvbio.2016.07.015
AOAC. 2000. Official method of analysis of the association of official analytical chemists. Washington D.C. 12, 377-378.
Arnon, D., 1949. Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiology. 24, 1-15.
Belal, B.E.A., El-Kenawy, M.A., Uwakiem, M.K., 2016. Foliar application of some amino acids and vitamins to improve growth, physical and chemical properties of flame seedless grapevines. Egyptian Journal of Horticulture. 43, 123-136. https://doi.org/10.21608/ EJOH.2016.2831
Bidaki, S., Tehranifar, A., Khorassani, R., 2018. Post-harvest Shelf-life extension of fruits of two strawberry (Fragaria× ananassa Duch.) cultivars with amino acids application in soilless culture system. Journal of Soil and Plant Interactions. 9,1-10.  [In Persian with English summary]. https://doi.org/10.29252/ejgcst.9.2.1
Cheng, B., Lian, H.F., Liu, Y.Y., Yu, X.H., Sun, Y.L., Sun, X.D., Liu, S.Q., 2016. Effects of selenium and sulfur on antioxidants and physiological parameters of garlic plants during senescence. Journal of Integrative Agriculture. 15, 566-572. https://doi.org/10.1016/S2095-3119(15)61201-1
Dehghan, G., Khoshkam, Z., 2012. Tin (II)-quercetin complex: Synthesis, spectral characterization and antioxidant activity. Food Chemistry. 131, 422-427. https://doi.org/10.1016/j.foodchem.2011.08.074
Djanaguiraman, M., Prasad, P. V., Seppanen, M., 2010. Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiology and Biochemistry. 48, 999-1007. https://doi.org/10.1016/j.plaphy.2010.09.009
Eom, S.H., Ahn, M.A., Kim, E., Lee, H.J., Lee, J.H., Wi, S.H., Kim, S.K., Lim, H.B., Hyun, T.K., 2022. Plant response to cold Stress: Cold stress changes antioxidant metabolism in heading type Kimchi cabbage (Brassica rapa L. ssp. Pekinensis). Antioxidants. 11, 700. https://doi.org/10.3390/antiox11040700
Erdal, S., 2012. Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiology and Biochemistry. 57, 1-7. https://doi.org/10.1016/j.plaphy.2012.04.016
Faten, S.A., Shaheen, A.M., Ahmed, A.A., Mahmoud, A.R., 2010. Effect of foliar application of amino acids as antioxidants on growth, yield and characteristics of Squash. Research Journal of Agriculture and Biological Science. 6, 583-588.
Guo, X., Li, J., Zhang, L., Zhang, Z., He, P., Wang, W., Wang, M., Wang, A., Zhu, J., 2020. Heterotrimeric G-protein α subunit (LeGPA1) confers cold stress tolerance to processing tomato plants (Lycopersicon esculentum Mill). BMC Plant Biology. 26; 20, 394. https://doi.org/10.1186/s12870-020-02615-w
Haghighi, M., Abolghasemi, R., da Silva, J. A.T., 2014. Low and high temperature stress affect the growth characteristics of tomato in hydroponic culture with Se and nano-Se amendment. Scientia Horticulturae. 178, 231-240. https://doi.org/10.1016/j.scienta.2014.09.006
Hawrylak-Nowak, B., Matraszek, R., Szymańska, M., 2010. Selenium modifies the effect of short-term chilling stress on cucumber plants. Biological Trace Element Research. 138, 307-315. https://doi.org/10.1007/s12011-010-8613-5
Huang, C., Qin, N., Sun, L., Yu, M., Hu, W., Qi, Z., 2018. Selenium improves physiological parameters and alleviates oxidative stress in strawberry seedlings under low-temperature stress. International Journal of Molecular Sciences. 19, 1913. https://doi.org/10.3390/ijms19071913
Jalili Marandi, R., 2004. Postharvest physiology (Handling and storage of fruits, vegetables and ornamental plants). Publishers Jihad Urmia University (2nd ed.). p. 276. [In Persian]
Javanmardi, J., Sattar, H., 2016. Evaluation of quantitative and qualitative characteristics of five greenhouse tomato cultivars in response to fertilizers containing seaweed extract and amino acids. Journal of Science and Technology of Greenhouse Culture. 7, 121-130. [In Persian with English summary]. https://doi.org/10.18869/acadpub.ejgcst.7.1.121
Kang, G., Wang, C., Sun, G., Wang, Z., 2003. Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environmental and Experimental Botany. 50, 9-15. https://doi.org/10.1016/S0098-8472(02)00109-0
Khalofah, A., Migdadi, H., El-Harty, E., 2021. Antioxidant enzymatic activities and growth response of quinoa (Chenopodium quinoa willd) to exogenous selenium application. Plants. 10, 719. https://doi.org/10.3390/plants10040719
Khan, S., Yu, H., Li, Q., Gao, Y., Sallam, B.N., Wang, H., Liu, P., Jiang, W., 2019. Exogenous application of amino acids improves the growth and yield of lettuce by enhancing photosynthetic assimilation and nutrient availability. Agronomy. 9, 266.  https://doi.org/10.3390/agronomy9050266
Khavari Nezhad, R.A., Goshehgir, Z. Saadatmand, S., 2010. The effects of selenium-molybdenum interaction on contents of photosynthetic pigments in tomato (Lycopersicom esculentum Mill.). Journal of Iranian Plant Ecophysiological Research. 5, 14-23. [In Persian with English abstract].
Kurepin, L.V., Ivanov, A.G., Zaman, M., Pharis, R.P., Allakhverdiev, S. I., Hurry, V., Hüner, N.P., 2015. Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynthesis Research. 126, 221-235. http://doi.org/10.1007/s11120-015-0125-x
Lee, G.J., Kang, B.K., Kim, T.I., Kim, T.J., Kim, J.H., 2007. Effects of different selenium concentrations of the nutrient solution on the growth and quality of tomato fruit in hydroponics. International Symposium on Advances in Environmental Control. 761, 443-448. https://doi.org/10.17660/ActaHortic.2007.761.61
Liang, W., Wang, M., Ai, X., 2009. The role of calcium in regulating photosynthesis and related physiological indexes of cucumber seedlings under low light intensity and suboptimal temperature stress. Scientia Horticulturae. 123(1), 34-38. https://doi.org/10.1016/j.scienta.2009.07.015
Liu, Q., Wang, D., Wu, G., Hao, G., Hao, Y., Sun, S. 2011. Effects of selenium on leaf senescence and antioxidase system in Pyrus bretschneider 'Dangshan Suli'. Acta Horticulturae Sinica. 38, 2059-2066.
Matysiak, K., Kierzek, R., Siatkowski, I., Kowalska, J., Krawczyk, R., Miziniak, W., 2020. Effect of exogenous application of amino acids l-arginine and glycine on maize under temperature stress. Agronomy. 10, 769.  https://doi.org/10.3390/agronomy10060769
Mesa, T., Polo, J., Arabia, A., Caselles, V., Munné-Bosch, S., 2022. Differential physiological response to heat and cold stress of tomato plants and its implication on fruit quality. Journal of Plant Physiology. 268, 153581. https://doi.org/10.1016/j.jplph.2021.153581
Moura, P.H.A., Coutinho, G., Pio, R., Bianchini, F.G., Curi, P.N., 2016. Plastic covering, planting density, and prunning in the production of Cape gooseberry (Physalis peruviana L.) in subtropical region. Revista Caatinga. 29, 367-374. http://doi.org/10.1590/1983-21252016v29n213rc
Mozaffari, M., Razavi, F., Rabiei, V., Kheiry, A., Hassani, A., 2020. Effect of preharvest spraying of selenium on qualitative and biochemical characteristics of grape cv. Fakhri (Vitis vinifera cv. Fakhri). Journal of Horticultural Science. 34, 61-74.  [In Persian with English summary]. https://doi.org/10.22067/JHORTS4.V33I4.79017
MSh, S., Orabi, S.A., Bakry, A.B., 2015. Antioxidant properties, secondary metabolites and yield as affected by application of antioxidants and banana peel extract on Roselle plants. American-Eurasian Journal of Sustainable Agriculture. 9, 93-104.
Muniz, J., Kretzschmar, A.A., Rufato, L., Pelizza, T.R., Rufato, A.D.R., Macedo, T.A.D., 2014. General aspects of physalis cultivation. Ciencia Rural. 44, 964-970.  https://doi.org/10.1590/S0103-84782014000600002
Nasibi, F., Heidari, T., Asrar, Z., Mansoori, H., 2013. Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger. Journal of Soil Science and Plant Nutrition. 13, 680-689. https://doi.org/10.4067/S0718-95162013005000054
Pezzarossa, B., Rosellini, I., Borghesi, E., Tonutti, P., Malorgio, F., 2014. Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics. Scientia Horticulturae. 165, 106-110. https://doi.org/10.1016/j.scienta.2013.10.029
Põldma, P., Moor, U., Tõnutare, T., Herodes, K., Rebane, R., 2013. Selenium treatment under field conditions affects mineral nutrition, yield and antioxidant properties of bulb onion (Allium cepa L.). Acta Scientiarum Polonorum Hortorum Cultus. 12, 167-181.
Portu, J., Gonzalez-Arenzana, L., Hermosín-Gutierrez, I., Santamaria, P., Garde-Cerdan, T., 2015. Phenylalanine and urea foliar applications to grapevine: Effect on wine phenolic content. Food Chemistry. 180, 55-63. https://doi.org/10.1016/j.foodchem.2015.02.008
Puccinelli, M., Malorgio, F., Pezzarossa, B., 2017. Selenium enrichment of horticultural crops. Molecules. 22, 933. https://doi.orG/10.3390/molecules22060933
Puccinelli, M., Malorgio, F., Terry, L.A., Tosetti, R., Rosellini, I., Pezzarossa, B., 2019. Effect of selenium enrichment on metabolism of tomato (Solanum lycopersicum) fruit during postharvest ripening. Journal of the Science of Food and Agriculture. 99, 2463-2472.
Quiterio-Gutiérrez, T., Ortega-Ortiz, H., Cadenas-Pliego, G., Hernández-Fuentes, A.D., Sandoval-Rangel, A., Benavides-Mendoza, A., Juárez-Maldonado, A., 2019. The application of selenium and copper nanoparticles modifies the biochemical responses of tomato plants under stress by Alternaria solani. International Journal of Molecular Sciences. 20, 1950. https://doi.org/10.3390/ijms20081950
Radyuk, M., Domanskaya, I., Shcherbakov, R., Shalygo, N., 2009. Effect of low above-zero temperature on the content of low-molecular antioxidants and activities of antioxidant enzymes in green barley leaves. Russian Journal of Plant Physiology. 56,175-180. https://doi.org/10.1134/S1021443709020058
Rahmani Samani, M., Pirbalouti, A.G., Moattar, F., Golparvar, A.R. 2019. L-Phenylalanine and bio-fertilizers interaction effects on growth, yield and chemical compositions and content of essential oil from the sage (Salvia officinalis L.) leaves. Industrial Crops and Products.137,1-8. https://doi.org/10.1016/j.indcrop.2019.05.019
Ramos, S. J., Faquin, V., Guilherme, L. R. G., Castro, E. M., Ávila, F. W., Carvalho, G. S., ... Oliveira, C. 2010. Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant, Soil and Environment. 56, 584-588. https://doi.org/10.17221/113/2010-PSE
Sanikhani, M., Akbari, A. and Kheiry, A. 2020. Effect of phenylalanine and tryptophan on morphological and physiological characteristics in colocynth (Citrullus colocynthis L.). Journal of Plant Process and Function. 9(35), 317-328. [In Persian with English summary]. https://dorl.net/dor/20.1001.1.23222727.1399.9.35.5.6
Sarojnee, D.Y., Navindra, B., Chandrabose, S., 2009. Effect of naturally occurring amino acid stimulants on the growth and yield of hot peppers (Capsicum annum L.). Journal of Animal and Plant Sciences. 5, 414 - 424.
Sayyari, M., Ghanbari, F., Fatahi, S., Bavandpour, F., 2013. Chilling tolerance improving of watermelon seedling by salicylic acid seed and foliar application. Notulae Scientia Biologicae. 5, 67-73. https://doi.org/10.15835/nsb.5.1.8293
Schiavon, M., dall’Acqua, S., Mietto, A., Pilon-Smits, E.A., Sambo, P., Masi, A. Malagoli, M., 2013. Selenium fertilization alters the chemical composition and antioxidant constituents of tomato (Solanum lycopersicon L.). Journal of Agricultural and Food Chemistry. 61, 10542-10554. https://doi.org/10.1021/jf4031822
Shehata, S.A., Abdel-Wahab, A., 2018. Influence of compost, humic acid and amino acids on sweet pepper growth, productivity and storage-ability. Middle East Journal of Applied Sciences. 8, 922-927.
Shehata, S.A., Hassan, H.A., Tawfik, A.A., Farag, M.F., 2016. Improving the productivity and quality of the cucumber crop grown under greenhouse conditions using some stimulants and spraying amino acids. Journal of Plant Production. 7, 385-392. https://doi.org/10.21608/JPP.2016.45373
Shekari, G., Javanmardi, J., 2017. Effects of foliar application pure amino acid and amino acid containing fertilizer on broccoli (Brassica oleracea L. var. italica) transplants. Advances in Crop Science and Technology. 5, 280. https://doi.org/10.4172/2329-8863.1000280
Shekari, L., Kamelmanesh, M. M., Mozafarian, M., Sadeghi, F., 2016. Beneficial effects of selenium on some morphological and physiological trait of hot pepper (Capsicum anuum). Journal of Horticultural Science. 29, 594-600. [In Persian with English summary]. https://doi.org/10.22067/JHORTS4.V29I4.32110
Sherzod, R., Yang, E.Y., Cho, M.C., Chae, S.Y., Kim, J.H., Nam, C.W., Chae, W.B., 2019. Traits affecting low temperature tolerance in tomato and its application to breeding program. Plant Breeding and Biotechnology. 7, 350-359. https://doi.org/10.9787/PBB.2019.7.4.350
Smirnoff, N., Wheeler, G.L., 2000. Ascorbic acid in plants: biosynthesis and function. Critical reviews in biochemistry and molecular biology. 35, 291-314. https://doi.org/10.1080/07352680091139231
Sogvar, O., Razavi, F., Rabiei, V. Gohari, G., 2020. Postharvest application of L‐cysteine to prevent enzymatic browning of “Stanley” plum fruit during cold storage. Journal of Food Processing and Preservation. 44, 14788. https://doi.org/10.1111/jfpp.14788
Teixeira, W.F., Fagan, E.B., Soares, L.H., Umburanas, R.C., Reichardt, K., Neto, D.D., 2017. Foliar and seed application of amino acids affects the antioxidant metabolism of the soybean crop. Frontiers in Plant Science. 8, 327. https://doi.org/10.3389/fpls.2017.00327
Vega, J.C.D.L., Olmedo, V., Ortega, C.G., Lara, M.V., Espin, R.D.C., 2020. Conservation advances on Physalis peruviana L. and Spondia purpurea: a review. Food Science and Technology. (AHEAD). https://doi.org/10.1590/fst.27520
Yadav, S. K., 2010. Cold stress tolerance mechanisms in plants. A review. Agronomy for Sustainable Development. 30, 515-527. https://doi.org/10.1051/agro/2009050
Yang, H., Chen, L., Zhou, C., Yu, X., Yagoub, A.E.A., Ma, H., 2018. Improving the extraction of l-phenylalanine by the use of ionic liquids as adjuvants in aqueous biphasic systems. Food Chemistry. 245, 346-352. https://doi.org/10.1016/j.foodchem.2017.10.110
Yang, Z.Q., Han, D., Wang, L., Jin, Z.F., 2016. Changes in photosynthetic parameters and antioxidant enzymatic activity of four tea varieties during a cold wave. Acta Ecologica Sinica. 36, 629-641.
Zhang, F., Lu, K., Gu, Y., Zhang, L., Li, W., Li, Z., 2020. Effects of low-temperature stress and brassinolide application on the photosynthesis and leaf structure of tung tree seedlings. Frontiers in Plant Science. 10, 1767. https://doi.org/10.3389/fpls.2019.01767