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Rowan, D. D., Cao, M., Lin-Wang, K., Cooney, J. M., Jensen, D. J., Austin, P. T., et al. (2009). Environmental regulation of leaf colour in red 35S:PAP1 arabidopsis thaliana. New Phytol. 182, 102–115. doi:10.1111/j.1469-8137.2008.02737.x In recent years, analytical methods such as multi-omics have been widely used in the study of food components and functions. To investigate flavonoid compositions in SOPs and elucidate the regulatory mechanism of flavonoid biosynthesis under magnesium stress, transcriptomic and metabolomic analyses were performed. Through these analyses, six hub candidate structural genes and ten hub TF genes involved in flavonoid biosynthesis regulation were identified using WGCNA and CCA. This valuable information enhances our understanding of the nutritional value of SOPs and provides insights into their potential use in food. Materials and methods Plants and sample preparation
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An investigation of differentially accumulated flavonoids (DAFs) was conducted in SOPs at different development stages. A total of 740 flavonoids were screened, and 142 DAFs were selected based on a fold change of |log2FC| ≥ 2 or |log2FC| ≤ 0.5 and a variable importance in projection (VIP ≥1) ( Supplementary Table4). Of these, 57 DAFs were identified in MS1 vs. MD1, followed by MS2 vs. MD2 (25) and MS3 vs. MD3 (97) ( Figure4C). The Venn Diagram results revealed two common and unique differential metabolites (Chrysoeriol-7-O-glucoside, Chrysoeriol-7-O-(6’’-feruloyl) glucoside) between MS and MD across all three periods. These flavonoids were flavones, and their change trend was consistent with total flavonoid content. To study the variation of these differential metabolites under magnesium stress, volcano diagrams were performed ( Supplementary Figure5). The results indicated that there were more up-regulated than down-regulated flavonoids in three stages between MS and MD. Specifically, 57 DAFs (53 upregulated and 4 downregulated) were identified during MS1 vs. MD1, 25 DAFs (6 upregulated and 19 downregulated) were identified during MS2 vs. MD2, and 97 DAFs (86 upregulated and 11 downregulated) were identified during MS3 vs. MD3. The majority of DAFs were observed during the development period. There were 278 DAFs (141 upregulated and 137 downregulated) and 261 DAFs (161 upregulated and 100 downregulated) selected from MD1 vs. MD2 and MS1 vs. MS2, respectively. The greater number of DAFs in MD than MS suggested that flavonoids may have been more susceptible to magnesium stress. The interaction of DAFs in SOPs resulted in the formation of different pathways, which were annotated and assigned to the KEGG pathways ( Figure4D). KEGG pathway enrichment analysis showed that flavonoid biosynthesis, phenylpropanoid biosynthesis, flavone and flavonol biosynthesis, secondary metabolites biosynthesis and metabolic pathways were the main enrichment pathways. Therefore, it could be postulated that the differentially accumulated metabolites (DAMs) in the pathways mentioned above may contribute to the variation in flavonoids of SOPs during the developmental process. Differentially expressed gene analysis
An improved protocol was used to determine the total flavonoid content of citrus peels ( Wang etal., 2007; Yu etal., 2022). Initially, 0.5 g citrus peel powder was weighed and dissolved in 10 mL 70% absolute ethanol at a ratio of 1:20 (w/v). The mixture was then subjected to ultrasonic treatment at 55°C for 40 min, followed by filtration. To 1 mL of the extraction solution, 0.5 mL of 5% NaNO 2 solution was added sequentially and well shaken. The mixture was then left for 5 min. Next, 0.5 mL 10% Al(NO 3) 3 was added to the solution, mixed thoroughly, and left for 6 min. Finally, 5 mL of 1mol/L NaOH was added, and distilled water was added up to 10 mL. The mixture was shaken and left for 10 min to complete the reaction. The absorbance value of solution was measured at 510 nm, with rutin (purity≥98%, sourced from Leaf Shanghai Biological Technology Co., Ltd.) used as the standard product. The flavonoid content (U mol/g) was calculated using the formula (C*V)/W, where C represents the concentration, V represents the volume, and W represents the weight of the sample. To determine the MDA content and SOD activity, Li’s method was followed ( Li etal., 2022b). Metabolomic profile detection and analysis Mahmoud, A. M., Hernandez Bautista, R. J., Sandhu, M. A., Hussein, O. E. (2019). Beneficial effects of citrus flavonoids on cardiovascular and metabolic health. Oxid. Med. Cell Longev 2019, 5484138. doi:10.1155/2019/5484138 Khare, S., Singh, N. B., Singh, A., Hussain, I., Niharika, K., Yadav, V., et al. (2020). Plant secondary metabolites synthesis and their regulations under biotic and abiotic constraints. J. Plant Biol. 63, 203–216. doi:10.1007/s12374-020-09245-7
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In GO annotation analysis, a total of 38,397 DEGs were annotated in three categories: biological process, molecular function, and cellular component categories ( Supplementary Table7). These DEGs were further divided into 47 categories based on gene function, with 722 genes related to biological processes such as signaling. TopGO analysis revealed that the most enriched molecular function terms were monooxygenase activity (GO0004497), oxidoreductase activity (GO0016705), heme binding (GO0020037), iron ion binding (GO0005506), and tetrapyrrole binding (GO0046906) ( Supplementary Figure7). The most enriched biological process terms were flavonoid metabolic process (GO0009812) and flavonoid biosynthetic process (GO0009813). The most enriched cellular component terms were chloroplast thylakoid (GO0009534) and plastid thylakoid (GO0031976). KEGG enrichment analysis identified the top 20 enriched metabolic pathways, including metabolic pathways (ko01100), biosynthesis of secondary metabolites (ko01110), MAPK signaling pathway-plant (ko04016), plant hormone signal transduction (ko04075), phenylpropanoid biosynthesis (ko00940), and flavonoid biosynthesis (ko00941) under magnesium stress ( Figure5D). These results were presented in a bubble diagram. Metabolic and gene co-expression networks in SOPs at different developmental stages Espley, R. V., Hellens, R. P., Putterill, J., Stevenson, D. E., Kutty-Amma, S., Allan, A. C. (2007). Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 49, 414–427. doi:10.1111/j.1365-313X.2006.02964.x Barreca, D., Gattuso, G., Bellocco, E., Calderaro, A., Trombetta, D., Smeriglio, A., et al. (2017). Flavanones: citrus phytochemical with health-promoting properties. Biofactors 43, 495–506. doi:10.1002/biof.1363 Bartwal, A., Mall, R., Lohani, P., Guru, S. K., Arora, S. (2013). Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J. Plant Growth Regul. 32, 216–232. doi:10.1007/s00344-012-9272-xTo date, efforts to identify the chemical compositions of citrus, especially flavonoid compounds, have increased significantly ( Barreca etal., 2017; Mahmoud etal., 2019; Yu etal., 2022). However, only a handful of flavonoid components present in citrus, specifically in SOPs, have been successfully identified. This limitation may hinder the growth of SOPs utilization in the food industry. Furthermore, flavonoids are a diverse group of plant metabolites that have diverse structures, wide distribution, and critical roles in plant growth, adaptation, signaling, and response to biotic and abiotic stresses ( Winkel-Shirley, 2001; Treutter, 2005; Rowan etal., 2009; Misra etal., 2010; Zhang etal., 2019). When the environment changes, flavonoid levels may also change. For example, Zanthoxylum bungeanum cv. “Fengjiao” exhibited an increase in total flavonoid content under drought stress ( Hu etal., 2021), while high solar radiation led to an increase in flavonol content in Ginkgo biloba ( Guo etal., 2020). In China, where citrus is mainly grown in subtropical and tropical regions, soil acidification and consequent magnesium (Mg) leaching are major problems ( Long etal., 2017). In addition, improper use of chemicals and inadequate use of organic fertilizers and medium and trace element fertilizers can lead to Mg deficiency in citrus, resulting in a decline in fruit quality and yield. Interestingly, Mg deficiency was found to increase total flavonoid content ( Ramakrishna and Ravishankar, 2011; Bartwal etal., 2013; Li etal., 2017; Khare etal., 2020). However, the underlying mechanism remains unexplored in SOPs. Liu, X. M., Hu, C. X., Liu, X. D., Riaz, M., Liu, Y., Dong, Z. H., et al. (2022). Effect of magnesium application on the fruit coloration and sugar accumulation of navel orange (Citrus sinensis osb.). Scientia Hortic. 304. doi:10.1016/j.scienta.2022.111282 Ahmed, O. M., Hassan, M. A., Abdel-Twab, S. M., Azeem, M. N. A. (2017). Navel orange peel hydroethanolic extract, naringin and naringenin have anti-diabetic potentials in type 2 diabetic rats. Biomed. Pharmacother. 94, 197–205. doi:10.1016/j.biopha.2017.07.094 Wang, Y., Liu, X. J., Chen, J. B., Cao, J. P., Li, X., Sun, C. D. (2022). Citrus flavonoids and their antioxidant evaluation. Crit. Rev. Food Sci. Nutr. 62, 3833–3854. doi:10.1080/10408398.2020.1870035
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