Phenylalanine and Calcium Nitrate Alleviate Cold Tolerance of Pistacia vera L. Seedlings

Subject Areas : Abiotic stress physiology

Mohammad  Fattah ¹ (Department of Horticulture, Damghan Branch, Islamic Azad University, Damghan, Iran)
Hossein  Afshari ² (Department of Horticulture, Damghan Branch, Islamic Azad University, Damghan, Iran)
Bahareh  Kashefi ³ (Department of Horticulture, Damghan Branch, Islamic Azad University, Damghan, Iran)
Ghanbar  Laei ⁴ (Department of Agriculture, Damghan Branch, Islamic Azad University, Damghan, Iran)
Vajiheh  Zarrinpour ⁵ (Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran)

Received: 2022-11-29 Accepted : 2023-05-03 Published : 2023-09-01

Keywords: Chlorophyll, Carotenoid, Proline, Cold stress, Pistacia vera L,

Abstract :

To study the effects of different concentrations of phenylalanine, and calcium nitrate under cold stress on Pistacia vera L. 'Abbas Ali' cultivar seedlings, a factorial experiment was performed with three factors of phenylalanine at three levels of calcium nitrate, and temperature based on a completely random design with three replications. The findings demonstrated that the effects of phenylalanine, calcium nitrate, temperature, as well as their interactions, were significant for all studied features. By simultaneous use of 2.5 mM of phenylalanine, and 5 ppm of calcium nitrate, electrolyte leakage reduced by 19% compared to the control sample at -3°C. Furthermore, when the temperature reduced from zero to -3°C, the concentration of proline increased from 2.3 to 3.1 μg g⁻¹ fw compared to the control seedlings. By simultaneous use of the highest concentrations of phenylalanine, and calcium nitrate, phenolic compounds, and soluble sugar increased. However, the interactions of phenylalanine×calcium nitrate, cold×phenylalanine, and phenylalanine×calcium nitrate×cold were not significant on the content of proline. A significant positive correlation was between proline, and soluble sugar at the probability level of 1% (r=0.87**). A significant negative correlation was between electrolyte leakage and chlorophyll fluorescence at the probability level of 1% (r=- 0.68**).

References:

Aazami MA, Asghari-Aruq M, Hassanpouraghdam MB, Ercisli S, Baron M, Sochor J (2021). Low Temperature stress mediates the antioxidants pool and chlorophyll fluorescence in Vitis vinifera L. cultivars. Plants. 10(9), 1877.

Alipour H (2018). Photosynthesis properties and ion homeostasis of different pistachio cultivar seedlings in response to salinity stress. International Journal of Horticultural Science and Technology. 5(1), 19-29.

Arjeh E, Akhavan HR, Barzegar M, Carbonell-Barrachina ÁA (2020). Bioactive compounds and functional properties of pistachio hull: A review. Trends in Food Science & Technology. 97, 55-64.

Arnon DI (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiology. 24, 1-15.

Ashraf M, Foolad MR (2007). Roles of glycine betaine and proline in improving plantabiotic strees resistance. Environmental and Exprimental Botany. 59, 206-2016.

Aslamarz AA, Vahdati K (2010). Stomatal density and ion leakage as indicators of cold hardiness in walnut. Acta Horticulturae. 861, 321-324.

Aslamarz AA, Vahdati K, Hasani D, Rahemi M, Leslie CA (2010) Supercooling and cold-hardiness in the acclimated and deacclimated buds and stems of Persian walnut cultivars and genotypes. HortScience. 45 (11), 1-6.

Aslani Aslamarz AA, Vahdati K, Hasani D, Rahemi M, Leslie CA (2011) Cold hardiness and its relationship with proline content in Persian walnut. European Journal of Horticultural Sciences. 76(3), 84–90.

Balasundram N, Sundram K, Samman S (2007). Phenolic compounds in plants and agri-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chemistry. 99, 191-203

Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K (2021) Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture. 11(8), 708.

Bertamini M, Zulini K, Muthuchelian K, Nedunchezhian N (2007). Low-night temperature effects on photosynthetic performance on two grapevine genotypes. Plant Biology. 51, 381-385.

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye Binding. Analytical Biochemistry. 72, 248- 254.

Chavoshi N, Marvizadeh MM, Fallah N, Rezaei-savadkouhi N, Mohammadi Nafchi N,  Marvizadeh S (2022). Application of Novel Nano-biopackaging Based on Cassava Starch/Bovine Gelatin/Titanium oxide nanoparticle/Fennel Essential Oil to Improve Quality of the Raw Fresh Pistachio. Journal of Nuts.  [In press].

Colom MR, Vazzana C (2001) Drought stress effects on three cultivars of Eragrostis curvula: photosynthesis and water relations. Plant Growth Regulation. 34, 195-202.

Cvetkovic J, Müller K, Baier M (2017). The effect of cold priming on the fitness of Arabidopsis thaliana accessions under natural and controlled conditions. Scientific report. 7(1), 1-16.

Erdal S (2012) Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiology and Biochemistry. 57, 1–7.

Ershadi A, Taheri S (2013). Effect of salicylic acid on spring frost tolerance of grape cultivar ‘Bidaneh Sefid’. Agricultural Crop Management (Journal of Agriculture). 15(2), 135-146. [In Persian]

Feng Q, Yang S, Wang Y, Lu L, Sun M, He C, et al. (2021). Physiological and molecular mechanisms of aba and CaCl₂ regulating chilling tolerance of cucumber seedlings. Plants. 10(12), 2746.

Garde-Cerdán T, López R, Portu J, González-Arenzana L, López-Alfaro I, Santamaría P (2014). Study of the effects of proline, phenylalanine, and urea foliar application to Tempranillo vineyards on grape amino acid content. Comparison with commercial nitrogen fertilisers. Food chemistry. 163, 136-141.

Gharib AL (2007). Effect of Salicylic Acid on the Growth, Metabolic Activities and Oil Content of Basil and Marjoram. International Journal of Agriculture and Biology. 2, 294-301.

Gharaghani A, Mohammadi Javarzaria A, Vahdati K (2018) Kaolin particle film alleviates adverse effects of light and heat stresses and improves nut and kernel quality in Persian walnut. Scientia Horticulturae. 239, 35–40.

Ghasemi-Soloklui AA, Ershadi A (2023) Screening pomegranate cultivars for freezing tolerance by reliable methods. International Journal of Horticultural Science and Technology. 10(2), 211-222.

Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek GN (2007). 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), 728-36.

Habibie A, Yazdani N, Saba MK, Vahdati K (2019). Ascorbic acid incorporated with walnut green husk extract for preserving the postharvest quality of cold storage fresh walnut kernels. Scientia Horticulturae. 245, 193-199.

Hassibi P, Moradi F, Nabipour M (2007). Screening of rice genotypes for low temperature stress-using chlorophyll fluorescence. Iranian Journal of Crop Sciences. 9, 14-31. [In Persian]

Hassegawa, RH, Fonseca, H, Fancelli AL, Dasilva VN, Schammass EA, Reis TA, Correa B 2008. Influence of macro and micro nutrient fertilization on fungal contamination and fumonisin production in corn grains. Food Control. 19, 36-43.

Hedge JE, Hofreiter BT (1962). In: whistler RL Be-Miller JN (Eds), Carbohydrate chemistry, Academic press, New York. pp. 211.

Hu ZR, Fan JB, Xie Y, Amombo E, Liu A, Gitau MM (2016). Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. Plant Physiology and Biochemistry. 100, 94–104.

Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S (2018). Chilling and drought stresses in crop plants: implications cross talk, and potential management opportunities. Frontiers in Plant Science. 9(393), 1-21.

Imlay JA, Linn S (1998). Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. Journal of Bacteriology. 169, 2967-2976.

Irigoyen JJ, Emerich DW, Diaz-Srganchie M (1992) Water stressinduced changeing concentrations of prolin and total soluble sugars inoculated alfalfa (Medicago sativa) plants. Physiologia Plantarum. 84, 67-72.

Isfendiyaroglu M, Zeker E (2002) The relation between phenolic compound and seed dormancy in Pistacia spp. In: AKB. E. (Ed.). 11 Grema Serr Pistachios and Almond. Chieres Optins Mediterraneenes. pp. 232-277.

Jackman RL, Yada RY, Marangoni A, Parkin KL, Stanley DW (1988). Chilling Injury. A review of quality aspects. Journal of Food Quality. 11, 253-278.

Kafi M, Mahdavi Damghani A (2002) Mechanisms of Environmental Stress Resistance in Plant (Translated). Published by Ferdowsi University Mashhad. Mashhad. pp. 472. [In Persian].

Khan TA, Fariduddin Q, Yusuf M (2017) Low-temperature stress: is phytohormones application a remedy? Environmental Science and Pollution Research. 24, (27) 21574-21590.

Khandan-Mirkoh A, Khalili Halbi M, Salami A, Lesani H (2017) Improving effects of mild cold stress and salicylic acid on growth and physiology of periwinkle (Catharanthus roseus Don.). International Journal of Horticultural Science and Technology. 4(1), 67-78.

Liu X, Huang B 2002. Cytokinin effects on creeping bentgrass response to heat stress. Crop Science. 42, 466-472.

Majdi M, Karimzade G, Mahfoozi S (2007) Effects of low temperature and exogenous calcium on the quantum efficiency of photosystem II (Fv/Fm) and relative content of chlorophyll in cold susceptible and tolerant wheat cultivars. Journal of Research and Development in Agriculture and Horticulture. 77, 175- 181. [In Persian].

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence a practical guide. Journal of Experimental Botany. 51, 659-668.

Mohammad Rezakhani S, Pakkish Z (2017) Influences of brassinosteroide and hot water on postharvest enzyme activity and lipid peroxidaion of lime (Citrus aurantifolia L.) fruit during storage at cold temperature. International Journal of Horticultural Science and Technology. 4(1), 57-65.

Moradmand Y, Mobli M, Ramin AA (2015) Effects of methyl jasmonate and salicylic acid on increasing cold tolerance of bell pepper (cv. Emily) seedlings. Journal of Crop Production and Processing. Isfahan University of Technology. 5 (16), 123-133. [In Persian]

Nasibi F, Manouchehri Kalantari K, Manzari Tavakoli Z (2020) Effects of hydrogen sulfide on cold-Induced oxidative damage in Cucumis sativus L. International Journal of Horticultural Science and Technology. 7(3), 199-211.

Nazoori F, ZamaniBahramabad E, Mirdehghan H (2022) Effect of Sulfur Pesticide on the Quality of Fresh Pistachio in Cold Storage. International Journal of Horticultural Science and Technology. 9(4), 453-462.

Nazoori F, ZamaniBahramabad E, Mirdehghan H, Yousefi M (2022) Preharvest application of sulfur as pesticide on fresh hull and kernel of pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9(1), 117-129.

Nobari A, Marvizadeh MM, Sadeghi T, Rezaei-savadkouhi N, Nafchi AM. (2022). Flavonoid and Anthocyanin Pigments Characterization of Pistachio Nut (Pistacia vera) as a Function of Cultivar. Journal of Nuts. 13(4), 313-22.

Norozi M, ValizadehKaji B, Karimi R, Nikoogoftar Sedghi M (2019).  Effects of foliar application of potassium and zinc on pistachio (Pistacia vera L.) fruit yield. Horticultural Science and Technology. 6(1), 113-23.

Paquin R, Lechasseur P 1979. Observation sur une method dosage I proline libre dans les extraits de plants. Canadia Journal of Botany. 57, 1851-1854.

Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiology and Biochemistry. 40, 141-150.

Portu J, González-Arenzana L, Hermosín-Gutiérrez I, Santamaría P, Garde-Cerdán T (2015) Phenylalanine and urea foliar applications to grapevine: Effect on wine phenolic content. Food Chemistry. 180, 55-63.

Ranney TG, Bassuk NL, Whitlow TH (1991). Osmotic adjustment and solute constituents in leaves and roots of water-stressed cherry (Prunus) trees. Journal of the American Society for Horticultural Science. 116, 684-688.

Repkina N, Ignatenko A, Holoptseva E, MiszalskI Z, Kaszycki P, Talanova V (2021). Exogenous methyl jasmonate improves cold tolerance with parallel induction of two cold-regulated (COR) genes expression in Triticum aestivum L. Plants. 10, 1421.

Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Science. 162, 897-904.

Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM (2008). Higher plant antioxidants and redox signaling under environmental stresses. Comptes Rendus Biologies. 331, 433–441.

Shamshiri MH, Hasani MR (2015) Synergistic accumulative effects between exogenous salicylic acid an arbuscular mycorrhizal fungus in pistachio (Pistacia Vera cv. Abareqi) seedlings under drought stress. International Journal of Horticultural Science and Technology. 2(2), 151-160.

Sharifkhah M, Bakhshi1 D, Pourghayoumi MR, Abdi S, Hokmabadi H (2020) Effect of pollination time on yield and antioxidant properties of some pistachio cultivars. International Journal of Horticultural Science and Technology. 7(1), 51-58.

Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiologia Plantarum 119(2), 253-262.

Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M., Pathre U. and Mohanty P. (Ed.). Probing photosynthesis: Mechanisms, Regulation and Adaptation, Tylor and Francis, New York. pp. 445-483.

Sun X, Zhu Z, Zhang L, Fang L, Zhang J, Wang Q, (2019) Overexpression of ethylene response factors VaERF080 and VaERF087 from Vitis amurensis enhances cold tolerance in Arabidopsis. Scientia Horticulturae. 243, 320– 326.

Tadjvar Y, Fotouhi Ghazvini R, Hamidoghli Y, Sajedi RH (2011) Physiological and biochemical responses of page mandarin on citrange rootstock to low temperature stress. Iranian Journal of Plant Biology. 3(9), 1- 12. [In Persian].

Taiz L, Zeiger E (2002) Plant Physiology. (2nd Ed.). Sinauer Associates, Inc., Publishers. Sunderland, Massachusetts. USA, pp. 764

Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiologia Plantarum. 126, 81-89.

Yokota H, Iehisa JCM, Shimosaka E, Takumi S (2015) Line differences in Cor/Lea and fructan biosynthesis-related gene transcript accumulation are related to distinct freezing tolerance levels in synthetic wheat hexaploids. Journal of Plant Physiology. 176, 78–88.

Zhang J, Kluera N, Wang Z, Ray W, Ho T, Nguyen H (2000) Genetic engineering for abiotic stress resistance in crop plants. In Vitro Cellular and Developmental Biology. 36, 108- 114.