Influence of gibberellic acid on primary metabolite accumulation in temperate [Lycoris radiata (L'Hér.) Herb.] grown in subtropical Terai region of West Bengal, India
Abstract
This study aimed to evaluate the impact of various gibberellic acid concentrations on the accumulation of primary metabolites like carbohydrates, proteins and lipids under the Terai region of West Bengal in Lycoris radiata, a temperate bulbous ornamental, which is known for its unique flowering and complexity of growth. Results revealed the higher accumulation of carbohydrates in 250 ppm of GA3 and 100 ppm of GA3 in leaves and bulbs respectively. Protein content peaked at 125 ppm in leaves and 250 ppm in bulbs and lipid levels were highest at 300 ppm in leaves and 175 ppm in bulbs. Result helps to figure out how gibberellic acid modulate the metabolic pathways to influence source-sink dynamics and storage physiology of this temperate species in non-temperate region like Terai region of West Bengal.
Full Text
Tables and figures are in the full-text PDF.
Introduction
[Lycoris radiata (L'Hér.) Herb.], also called as Spider Lily (Chang et al., 2009) [5] or Magic Lily or Hurricane Lily (Yang et al., 2023) [17] is a temperate ornamental geophyte (Cai et al., 2020) [4] , belonging to the plant family Amaryllidaceae and native to Asian countries like Japan, China, Korea and Nepal (Cahlikova et al., 2020) [2] . It is widely naturalized in China (Liu et al., 2016) [11] and introduced to Japan along with paddy cultivation as a companion crop (Hayashi et al., 2005) [8] . The Netherlands, world leading producer of ornamental geophytes, also leads in the production of Lycoris radiata, where its cultivation is being practiced over 60ha (Cai et al., 2019) [3] . Due to the peculiar growth pattern and attracting unique inflorescence (Cheng et al., 2022) [6] , it is gaining popularity in cut flower industry, as a potted plant and in landscape gardening. Since it is a temperate species, where it requires 13-22 °C for floral transition (Cai et al., 2019) [3] , it seems to be quite challenging to grow in subtropical regions like Terai plains of West Bengal. Among the different plant growth regulators, gibberellic acid (GA3) has the potentiality to induce flowering in temperate ornamental geophytes, which is already proven in crops, like-Tulips, Liliums, Ornithogalum etc. (Gul et al., 2020) [7] . Gibberellic acid interacts with DELLA protein, a negative regulator of floral transition and degrades it through ubiquitination pathway, thereby, allowing the phase shifting of plants from vegetative to reproductive (Wang and Deng, 2011) [15] . Gibberellic acid also known to increase the levels of primary metabolites, like-carbohydrates, proteins and lipids (Murcia et al., 2017) [12] , in geophytes and make them more metabolically active. An experiment was conducted in the Terai region of West Bengal to evaluate the effect of different concentrations of gibberellic acid on the accumulation of primary metabolites, like-carbohydrate, protein and lipid in both leaves as well as in bulbs of Lycoris radiata.
Materials and Methods
The experiment was conducted at the Instructional Farm of Department of Floriculture, Medicinal and Aromatic Plants, Faculty of Horticulture, Uttar Banga Krishi Viswavidyalaya, Pundibari, CoochBehar, India in 2021-22 The experiment was laid in Completely Randomized Block Design, with three replications and thirteen treatments of gibberellic acid-viz., T1-0 ppm of GA3, T2-25 ppm, T3-50 ppm, T4-75 ppm of GA3, T5-100 ppm of GA3, T6-125 ppm of GA3, T7-150 ppm of GA3, T8-175 ppm of GA3, T9-200 ppm of GA3, T10-225 ppm of GA3, T11-250 ppm of GA3, T12-275 ppm of GA3 and T13-300 ppm of GA3. The bulbs of Lycoris radiata were collected form ICAR-IARI Regional Station, Kalimpong and dipped in different concentrations of gibberellic acid for six hours before planting and also applied as foliar sprays at monthly interval. The estimation of carbohydrate content was performed by using Anthrone method (Yemm and Willis, 1954) [18] , protein by Lowry's method (Waterborg and Matthews, 1994) [16] and Lipid content using Automatic Solven Extraction (Schafer, 1998) [14] using petroleum ether as a solvent.
Results and Discussion
The effect of gibberellic acid on various biochemical parameters of Lycoris radiata showed statistically significant results and it was found that the accumulation was higher in bulbs than the leaves. Among the different treatments of gibberellic acid, application of 250 ppm of GA3 showed the maximum carbohydrate content (7.93 g/100 g) in leaves, while in bulbs, the higher accumulation (23.61 g/100 g) was observed with the application of 100 ppm of GA3. The least amount of carbohydrate was estimated in control (0 ppm of GA3) (2.93 g/100 g) in leaves and in 275 ppm of GA3 (13.76 g/100 g) in bulbs. In the protein content, highest accumulation (0.212 g/100 g) in leaves was observed in 125 ppm of GA3, whereas, the least content (0.154 g/100 g) was showed in control. In the bulbs, higher protein content (0.792 g/100 g) was observed in 250 ppm of GA3 and least content (0.337 g/100 g) in 75 ppm of GA3. Regarding the lipid content, higher concentration (300 ppm of GA3) resulted more amount of lipid accumulation in leaves (0.373 g/100 g), while in the bulbs, 175 ppm of GA3 showed the highest lipid content (5.02 g/100 g), on the other hand, the lower amount of lipid content resulted in control plants in both the leaves (0.177 g/100 g) as well as in bulbs (1.08 g/100 g). Differences in accumulation of primary metabolites have been observed with the exogenous application of gibberellic acid in Lycoris radiata. Among the various concentrations, 250 ppm of GA3 in leaves and 100 ppm of GA3 in bulbs showed the maximum accumulation of carbohydrate content and these specific concentrations might have increased the photosynthetic activity leading to higher accumulation of carbohydrate in leaves (Yuan and Xu, 2001) [19] . Interestingly, the lower concentration, like-100 ppm showed more accumulation in bulbs, possibly due to high phloem loading and translocation of photoassimilates from source (leaves) to sink (bulbs) (Murcia et al., 2016) [13] . GA3 has the ability to influence nitrogen metabolism and protein biosynthesis by regulating key enzymes like nitrate reductase and glutamine synthetase (Higgins et al., 1982). Intermediate concentration like 125 pppm of GA3 might have elevated the amino acid synthesis and thereby increasing the protein content in leaves. However, higher concentration, like-250 ppm of GA3 might have delayed the accumulation in leaves, but increased the deposits of nitrogenous compounds in storage tissues. Lipids are the energy-dense biomolecules and are essential for membrane synthesis (Byrnes et al., 2022) [1] that serves as a long-term energy source in most of the geophytes. The elevated lipid content at highest concentration (300 ppm of GA3) in leaves, might be due to upregulation of acetyl-coA carboxylase enzyme, which involved in fatty acid biosynthesis (Kresnawaty et al., 2023) [10] . Whereas, moderate concentration (175 ppm of GA3) showed more accumulation of GA3 in bulbs and this suggests that increased concentrations prioritize vegetative growth over the storage accumulation.
Conclusion
The differential accumulation of primary metabolites across the leaf and bulb tissues of Lycoris radiata, shows the concentration specific response of exogenous application of gibberellic acid. 250 ppm of GA3 enhanced the carbohydrate and protein content in leaves and bulbs respectively, while lipid accumulation was more in 300 ppm in leaves and 175 ppm in bulbs. These findings revealed the role of GA3 in partitioning of primary metabolites to finetune the vegetative growth and storage functions and paved a way to understand the physiological behaviour of this temperate species to various concentrations of gibberellic acid under the Terai region of West Bengal.
References
- Byrnes K, Blessinger S, Bailey NT, Scaife R, Liu G, Khambu B. Therapeutic regulation of autophagy in hepatic metabolism. Acta Pharmaceutica Sinica B. 2022;12(1):33-49.
- Cahlikova L, Breiterová K, Opletal L. Chemistry and biological activity of alkaloids from the genus Lycoris (Amaryllidaceae). Molecules. 2020;25(20):1-20.
- Cai J, Fan J, Wei X, Zhang L. A three-dimensional analysis of summer dormancy in the red spider lily (Lycoris radiata). HortScience. 2019;54(9):1459-1464.
- Cai J, Fan J, Wei X, Zhang D, Ren J, Zhang L. Differences in floral development between Lycoris radiata a n d Lycoris sprengeri. ScienceAsia. 2020;46:271-279.
- Chang YC, Shii CT, Chung MC. Variations in ribosomal RNA gene loci in spider lily (Lycoris spp.). Journal of the American Society for Horticultural Science. 2009;134(5):567-573.
- Cheng G, Zhang F, Shu X, Wang N, Wang T, Zhuang W, et al. Identification of differentially expressed genes related to floral bud differentiation and flowering time in three populations of Lycoris radiata. International Journal of Molecular Sciences. 2022;23(22):1-24.
- Gul F, Shahri W, Tahir I. Bulbous ornamentals: Role and scope in the floriculture industry. In: The Global Floriculture Industry. Apple Academic Press; 2020. p. 15-38. ISBN: 978-1-77188-878-3.
- H a y a s h i A , S a i t o T , M u k a i Y , K u r i t a S , H o r i T A . Genetic variations in Lycoris radiata var. radiata in Japan. Genes and Genetic Systems. 2005;80(3):199212.
- Higgins TJ, Jacobsen JV, Zwar JA. Gibberellic acid and abscisic acid modulate protein synthesis and mRNA levels in barley aleurone layers. Plant Molecular Biology. 1982;1:191-215.
- Kresnawaty I, Santoso D, Permatasari GW, Hudiyono S. Gibberellic acid (GA) role in acetyl-CoA carboxylase enzyme regulation and in improving oil palm yield. Menara Perkebunan. 2023;91(2):130-139.
- Liu YX, Zheng YH, Xia T, Zhou J. Karyotype studies on Lycoris radiata populations from China. Genetics and Molecular Research. 2016;15(1):15017357.
- Murcia G, Fontana A, Pontin M, Baraldi R, Bertazza G, Piccoli PN. ABA and GA3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phytochemistry. 2017;135:34-52.
- Murcia G, Pontin M, Reinoso H, Baraldi R, Bertazza G, Gómez-Talquenca S, et al. ABA and GA3 increase carbon allocation in different organs of grapevine plants by inducing accumulation of non-structural carbohydrates in leaves, enhancement of phloem area and expression of sugar transporters. Physiologia Plantarum. 2016;156(3):323-337.
- Schafer K. Accelerated solvent extraction of lipids for determining the fatty acid composition of biological material. Analytica Chimica Acta. 1998;358(1):69-77.
- Wang F, Deng XW. Plant ubiquitin-proteasome pathway and its role in gibberellin signaling. Cell Research. 2011;21(9):1286-1294.
- Waterborg JH, Matthews HR. The Lowry method for protein quantitation. In: Basic Protein and Peptide Protocols. New Jersey: Humana Press; 1994. p. 1-4.
- Yang S, Li Z, Fu L, Zheng Y, Huang Y, Zhang P. Lycoris 'Tao Hong': A new ornamental Lycoris hybrid cultivar. HortScience. 2023;58(8):935-936.
- Yemm EW, Willis A. The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal. 1954;57(3):508-514.
- Yuan L, Xu DQ. Stimulation effect of gibberellic acid short-term treatment on leaf photosynthesis related to the increase in Rubisco content in broad bean and soybean. Photosynthesis Research. 2001;68:39-47.
How this paper connects to the literature. Drag to explore, click any node to open that paper.
