Sains Malaysiana 52(4)(2023): 1161-1171

http://doi.org/10.17576/jsm-2023-5204-10

Gibberellic Acid Supplements Mitigate the Sodium Chloride Effects on Onion Seed Germination and Its Physio-Chemical Attributes

(Suplemen Asid Giberelik Mengurangkan Kesan Natrium Klorida pada Percambahan Biji Bawang dan Atribut Fisio-Kimianya)

IKRAM-UL HAQ¹, NAZIA PARVEEN GILL², GHULAM YASIN³, SAHIFA MEMON¹, ZAINAB SOOMRO¹, FAHEEM AHMED BHATTI^1,4, MEHWISH BALOCH¹ & CHANDA BAKHTAWAR BALOCH¹

¹Institute of Biotechnology and Genetic Engineering (IBGE), University of Sindh, Jamshoro-76080, Pakistan

²Department of Statistics, University of Sindh, Jamshoro-76080, Pakistan

³Department of Botany, Bahauddin Zakariya University, Multan-60800, Pakistan

⁴Sindh Agriculture Department, Tandojam-70060, Pakistan

Received: 3 July 2022/Accepted: 17 March 2023

Abstract

The mitigative effect of gibberellic acid (GA₃) for salt (NaCl) stresses on seed germination attributes of onion (Allium cepa L.) cultivar Nasarpuri was assessed. Seeds were moisturized with NaCl (0-, 100- and 200-mM) and GA₃ (250 ppm) before and after sowing for seed germination in 1^st week than in 2^nd week, GA₃ sprayed once foliarly and NaCl in rooting region. At the end of 1^st week, an increase in seed germination rate was observed in seeds supplemented with GA₃ from control (85.0%) to 97.5% and from NaCl stressed seeds (72.5% and 50.0%) to 85.0% and 62.5%, respectively (p ≤ 0.05). This reduction in seed germination was caused by salt stresses after 96th hours of sowing, inhibition in GA₃-biosynthesis GA₃ and delay in α-amylases activation observed in salt stressed seed cultures. The seedling vigor index (SVI) was observed higher in foliarly GA₃ sprayed cultures of both control as well as saline stressed cultures. The seedlings supplemented with GA₃, decrease in malondialdehyde (MDA), H₂O₂, Na⁺/K⁺, Na⁺ and Cl^- contents, while increases seedling biomass, chlorophyll contents, total proteins, and sugars in NaCl stressed seedlings. Interestingly, GA₃ also increased (p ≤ 0.05) the osmoprotectants in seedlings including abscisic acid (AsA), carotenoids, phenolics and proline contents to depict in stress alleviation. This study may be concluded by the fact that GA₃ minimizes salinity stresses on seed germination as well as further seedling growth with the increased production of organic osmoprotectants as saline stress neutralizers.

Keywords: Allium cepa L.; antioxidative responses; gibberellic acid (GA₃); H₂O₂ contents; saline stresses

Abstrak

Kesan mitigasi asid giberelik (GA₃) untuk garam (NaCl) menegaskan sifat percambahan benih bawang (Allium cepa L.) kultivar Nasarpuri telah dinilai. Benih telah dilembapkan dengan NaCl (0-, 100- dan 200-mM) dan GA₃ (250 ppm) sebelum dan selepas disemai untuk percambahan benih pada minggu pertama berbanding minggu ke-2, GA₃ disembur sekali pada daun dan NaCl di kawasan pengakaran. Pada akhir minggu pertama, peningkatan kadar percambahan biji benih diperhatikan pada benih yang ditambah dengan GA₃ daripada kawalan (85.0%) kepada 97.5% dan daripada benih bertekanan NaCl (72.5% dan 50.0%) kepada 85.0% dan 62.5% masing-masing (p). ≤ 0.05). Pengurangan dalam percambahan benih ini disebabkan oleh tegasan garam selepas 96 jam penyemaian, perencatan dalam GA₃-biosintesis GA₃ dan kelewatan dalam pengaktifan α-amilase yang diperhatikan dalam kultur benih bertekanan garam. Indeks vigor ankak benih (SVI) diperhatikan lebih tinggi dalam kultur semburan GA₃ daun bagi kedua-dua kawalan dan juga kultur bertekanan garam. Anak benih yang ditambah dengan GA₃ mengurangkan kandungan malondialdehid (MDA), H₂O₂, Na+/K+, Na+ dan Cl-, sambil meningkatkan biojisim anak benih, kandungan klorofil, jumlah protein dan gula pada anak pokok bertekanan NaCl. Menariknya, GA₃ juga meningkatkan (p ≤ 0.05) osmopelindung dalam anak benih termasuk kandungan asid absisik (AsA), karotenoid, fenol dan prolin untuk menggambarkan pengurangan tekanan. Kajian ini boleh disimpulkan oleh fakta bahawa GA₃ meminimumkan tegasan kemasinan pada percambahan biji benih serta pertumbuhan anak benih selanjutnya dengan peningkatan pengeluaran osmopelindung organik sebagai peneutral tegasan garam.

Kata kunci: Allium cepa L.; asid giberelik (GA₃); gerak balas antioksidatif; kandungan H₂O₂, tegasan garam

REFERENCES

Abbas, S. & Waheed, A. 2021. Fiscal deficit and trade deficit nexus in Pakistan: An econometric inquiry. Panoeconomicus 68(5): 745-763.

Aglaia, L., Georgios, Z., Theodoros, V. & Ioannis, N. 2011. Effect of NaCl and GA₃ on seed germination and seedling growth of eleven medicinal and aromatic crops. Journal of Medicinal Plants Research 5(17): 4065-4073.

Ahanger, M., Qin, C., Maodong, Q., Dong, X., Ahmad, P., Abd-Allah, E. & Zhang, L. 2019. Spermine application alleviates salinity induced growth and photosynthetic inhibition in Solanum lycopersicum by modulating osmolyte and secondary metabolite accumulation and differentially regulating antioxidant metabolism. Plant Physiology and Biochemistry 144: 1-13.

Ahmad, S., Cui, W., Kamran, M., Ahmad, I., Meng, X., Wu, X., Su, W., Javed, T., ElSerehy, H.A., Wu, X. & Jia, Z. 2021. Exogenous application of melatonin induces tolerance to salt stress by improving the photosynthetic efficiency and antioxidant defense system of maize seedling. Journal of Plant Growth Regulation 40(3): 1270-1283.

Ali, M., Hossain, M., Zakaria, M., Hossain, T., Naznin, A. & Islam, M. 2015. Effect of GA₃ on quality seed production of onion in Bangladesh. Ecofriendly Agricultural Journal 8(03): 47-50.

Allakhverdiev, S., Sakamoto, A., Nishiyama, Y., Inaba, M. & Murata, N. 2000. Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiology 123(3): 1047-1056.

Arnon, D. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24(1): 1-15.

Azam, A. & Shafique, M. 2017. Agriculture in Pakistan and its impact on economy. International Journal of Advanced Science and Technology 103: 47-60.

Bates, L.S., Waldren, R.P. & Teare, I.J.P. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil 39(1): 205-207.

Belaqziz, R., Romane, A. & Abbad, A. 2009. Salt stress effects on germination, growth and essential oil content of an endemic thyme species in Morocco (Thymus maroccanus Ball.). Journal of Applied Sciences Research 5(July): 858-863.

Brennan, T. & Frenkel, C. 1977. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiology 59(3): 411-416.

Caliński, T. 1981. Principles and procedures of statistics: A biometrical approach. Biometrics 37(4): 859-860. doi:10.2307/2530180 

Camara, M., Vandenberghe, L., Rodrigues, C., de Oliveira, J., Faulds, C., Bertrand, E. & Soccol, C. 2018. Current advances in gibberellic acid (GA₃) production, patented technologies and potential applications. Planta 248(5): 1049-1062.

Catsky, J. 1974. Water content. In Methods of Studying Plant Water Relations. Berlin: Springer-Verlag. pp. 121-131.

Chapman, H. & Pratt, P. 1961. Method of Analysis for Soils, Plants and Waters. University of California (Riverside), Division of Agriculture Sciences.

Chauhan, A., Abu Amarah, B., Kumar, A., Verma, J., Ghramh, H., Khan, K. & Ansari, M. 2019. Influence of gibberellic acid and different salt concentrations on germination percentage and physiological parameters of oat cultivars. Saudi Journal of Biological Sciences 26(6): 1298-1304.

Colomer-Winter, C., Flores-Mireles, A., Baker, S., Frank, K., Lynch, A., Hultgren, S., Kitten, T. & Lemos, J. 2018. Manganese acquisition is essential for virulence of Enterococcus faecalis. PLoS Pathogens 14(9): e1007102.

Dar, Z., Dar, S., Khan, J., Lone, A., Langyan, S., Lone, B., Kanth, R.H., Iqbal, A., Rane, J., Wani, S.H., Alfarraj, S., Alharbi, S.A., Brestic, M. & Ansari, M. 2021. Identification for surrogate drought tolerance in maize inbred lines utilizing high-throughput phenomics approach. PLoS ONE 16(7): e0254318.

Dubois, M., Gilles, K., Hamilton, J., Rebers, P. & Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28(3): 350-356.

FAO. 2021. FAOSTAT. Food and Agriculture Organization of the United Nations. Rome: FAO.

Gharib, F., Zeid, I., Ghazi, S. & Ahmed, E. 2018. Physiological effects of ascorbic and gallic acids on growth and metabolic activities of cowpea (Vigna unguiculata L.) plants. Journal of Plant Physiol. and Pathology 6(4): 2-9.

Ghodrat, V. & Rousta, M. 2012. Effect of priming with gibberellic acid (GA₃) on germination and growth of corn (Zea mays L.) under saline conditions. International Journal of Agriculture and Crop Sciences 4(13): 882-885.

Hamayun, M., Khan, S., Khan, A., Shin, J., Ahmad, B., Shin, D. & Lee, I. 2010. Exogenous gibberellic acid reprograms soybean to higher growth and salt stress tolerance. Journal of Agricultural and Food Chemistry 58(12): 7226-7232.

Heath, R. & Packer, L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125(1): 189-198.

Hillel, D., Braimoh, A. & Vlek, P. 2008. Soil degradation under irrigation. In Land Use and Soil Resources. Springer. pp: 101-119.

Ibrahim, M., Ali, A., Elsiddig, A., Zhou, G., Nimir, N., Agbna, G. & Zhu, G. 2021. Mitigation effect of biochar on sorghum seedling growth under salinity stress. Pakistan Journal of Botany 53(2): 387-392.

Ibrahim, M., Zhu, X., Zhou, G., Ali, A., Ahmad, I. & Farah, G. 2018. Nitrogen fertilizer alleviated negative impacts of NaCl on some physiological parameters of wheat. Pakistan Journal of Botany 50(6): 2097-2104.

Javid, M., Sorooshzadeh, A., Moradi, F., Modarres, S., Mohammad, S. & Allahdadi, I. 2011. The role of phytohormones in alleviating salt stress in crop plants. Australian Journal of Crop Science 5(6): 726-734.

Kadayifci, A., Tuylu, G., Ucar, Y. & Cakmak, B. 2005. Crop water use of onion (Allium cepa L.) in Turkey. Agricultural Water Management 72(1): 59-68.

Kandil, A., Sharief, A., Abido, W. & Awed, A. 2014. Effect of gibberellic acid on germination behaviour of sugar beet cultivars under salt stress conditions of Egypt. Sugar Tech 16(2): 211-221.

Kaur, S., Gupta, A. & Kaur, N. 1998. Gibberellin A₃ reverses the effect of salt stress in chickpea (Cicer arietinum L.) seedlings by enhancing amylase activity and mobilization of starch in cotyledons. Plant Growth Regulation 26(2): 85-90.

Law, M., Charles, S. & Halliwell, B. 1983. Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochemical Journal 210(3): 899-903.

Lerner, H.R. & Amzallag, G.N. 1994. The response of plants to salinity: A working hypothesis. In Biochemical and Cellular Mechanisms of Stress Tolerance in Plants, edited by Cherry, J.H. NATO ASI Series, vol 86. Berlin, Heidelberg: Springer. pp: 463-476.

Lima, M. & Leonardo, T. 2008. Onion production in salinized soil. Brazilian Journal of Agricultural and Environmental Engineering 12: 231-235.

Lin, J. & Stafford, A. 1987. Comparison of the endogenous gibberellins in the shoots and roots of vernalized and non-vernalized Chinese Spring wheat seedlings. Phytochemistry 26(9): 2485-2488.

Liu, L., Xia, W., Li, H., Zeng, H., Wei, B., Han, S. & Yin, C. 2018. Salinity inhibits rice seed germination by reducing α-amylase activity via decreased bioactive gibberellin content. Frontiers in Plant Science 9: 275.

Lowry, O. & Rosebrough, N. 1951. Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193(1): 265-275.

Lutts, S., Kinet, J. & Bouharmont, J. 1996. NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany 78(3): 389-398.

Machado, R. & Serralheiro, R. 2017. Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3(2): 30.

Mahender, A., Anandan, A. & Pradhan, S. 2015. Early seedling vigour, an imperative trait for direct-seeded rice: An overview on physio-morphological parameters and molecular markers. Planta 241(5): 1027-1050.

Majcherczyk, A., Rakoczy, L. & Huttermann, A. 1986. Improvements in methods for determination of abscisic acid and indole-3-acetic acid by high-performance liquid chromatography. Journal of Chromatography 357: 399-408.

Manniche, L. 1989. An Ancient Egyptian Herbal University of Texas Press Austin. Vol. 163.

Marles, R. & Farnsworth, N. 1995. Antidiabetic plants and their active constituents. Phytomedicine 2(2): 137-189.

Mbarki, S., Skalicky, M., Vachova, P., Hajihashemi, S., Jouini, L., Zivcak, M., Tlustos, P., Brestic, M., Hejnak, V. & Khelil, A.Z. 2020. Comparing salt tolerance at seedling and germination stages in local populations of Medicago ciliaris L. to Medicago intertexta L. and Medicago scutellata L. Plants 9(4): 526.

Miller, G. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31(3): 426-428.

Moons, A., Bauw, G., Prinsen, E., Van Montagu, M. & Van-Der, S.D. 1995. Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant Indica rice varieties. Plant Physiology 107(1): 177-186.

Munns, R., Schachtman, D. & Condon, A. 1995. The significance of a two-phase growth response to salinity in wheat and barley. Functional Plant Biology 22(4): 561-569.

Nasri, N., Maatallah, S., Saidi, I. & Lachaal, M. 2017. Influence of salinity on germination, seedling growth, ion content and acid phosphatase activities of Linum usitatissimum L. Journal of Animal and Plant Sciences 27(2): 517-521.

Nawaz, K., Hussain, K., Majeed, A., Khan, F., Afghan, S. & Ali, K. 2010. Fatality of salt stress to plants: Morphological, physiological and biochemical aspects. African Journal of Biotechnology 9(34): 5475-5480.

Negrao, S., Schmöckel, S. & Tester, M. 2017. Evaluating physiological responses of plants to salinity stress. Annals of Botany 119(1): 1-11.

Nounjan, N. & Theerakulpisut, P. 2012. Effects of exogenous proline and trehalose on physiological responses in rice seedlings during salt-stress and after recovery. Plant Soil and Environment 58(7): 309-315.

Parida, A., Das, A. & Mittra, B. 2004. Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees Structure and Function 18(2): 167-174.

Rahman, M., Haque, M., Karim, M. & Ahmed, M. 2006. Effects of gibberellic acid (GA₃) on breaking dormancy in garlic (Allium sativum L.). International Journal of Agriculture and Biology 8(1): 63-65.

Roychoudhury, A., Basu, S. & Sengupta, D. 2009. Effects of exogenous abscisic acid on some physiological responses in a popular aromatic Indica rice compared with those from two traditional non-aromatic Indica rice cultivars. Acta Physiologiae Plantarum 31(5): 915-926.

Salih, E., Zhou, G., Muddathir, A., Ibrahim, M., Ahmed, N., Ali, A., Ashraf, N.A. & Ahmad, I. 2022. Effects of seeds priming with plant growth regulators on germination and seedling growth of hargel (Solenostemma argel (Del.) Hayne) under salinity stress. Pakistan Journal of Botany 54(5): 1579-1587.

Srivastava, N. & Srivastava, A. 2007. Influence of gibberellic acid on ¹⁴CO₂ metabolism, growth, and production of alkaloids in Catharanthus roseus. Photosynthetica 45(1): 156-160.

Steel, R.G.D. & Torrie, J.H. 1980. Principles and Procedures of Statistics, A Biometrical Approach. McGraw-Hill Kogakusha, Ltd.

Sumner, J. 2019. Plants Go to War: A Botanical History of World War II. Jefferson, North California: McFarland and Company, Inc.

Takemura, T., Hanagata, N., Sugihara, K., Baba, S., Karube, I. & Dubinsky, Z. 2000. Physiological and biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. Aquatic Botany 68(1): 15-28.

Ti, H., Li, Q., Zhang, R., Zhang, M., Deng, Y., Wei, Z., Chi, J. & Zhang, Y. 2014. Free and bound phenolic profiles and antioxidant activity of milled fractions of different indica rice varieties cultivated in southern China. Food Chemistry 159: 166-174.

Tuna, A., Kaya, C., Dikilitas, M. & Higgs, D. 2008. The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environmental and Experimental Botany 62(1): 1-9.

Turner, N. 1981. Techniques and experimental approaches for the measurement of plant water status. Plant and Soil 58(1): 339-366.

Vetrano, F., Moncada, A. & Miceli, A. 2020. Use of gibberellic acid to increase the salt tolerance of leaf lettuce and rocket grown in a floating system. Agronomy, MDPI 10(4): 505.

Waterborg, J. 2009. The Lowry method for protein quantitation. In The Protein Protocols Handbook. Springer. pp: 7-10.

Wellburn, A. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144(3): 307-313.

Wu, Y., Jin, X., Liao, W., Hu, L., Dawuda, M., Zhao, X., Liu, J., Li, S., Wang, D., Guan, H. &Yu, J. 2018. 5-Aminolevulinic acid (ALA) alleviated salinity stress in cucumber seedlings by enhancing chlorophyll synthesis pathway. Frontiers in Plant Science 9: 635.

Yurekli, F., Porgali, Z. & Turkan, I. 2004. Variations in abscisic acid, indole-3-acetic acid, gibberellic acid and zeatin concentrations in two bean species subjected to salt stress. Acta Biologica Cracoviensia Series Botanica 46: 201-212.

Zhang, J. & Zhang, X. 1994. Can early wilting of old leaves account for much of the ABA accumulation in flooded pea plants? Journal of Experimental Botany 45(9): 1335-1342.

^*Corresponding author; email: rao.ikram@yahoo.com