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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 CiT Galaxy White Mid-Tower PC Gaming Case with 1 x LED Strip 1 x 120mm Rainbow RGB Fan Included Tempered Glass Side Panel Garcia, C., Arroyo, J. M., Godoy, J. A., Jordano, P. (2005). Mating patterns, pollen dispersal, and the ecological maternal neighbourhood in a prunus mahaleb l. population. Mol. Ecol. 14, 1821–1830. doi:10.1111/j.1365-294X.2005.02542.x Deng, Y. X., Lu, S. F. (2017). Biosynthesis and regulation of phenylpropanoids in plants. Crit. Rev. Plant Sci. 36, 257–290. doi:10.1080/07352689.2017.1402852

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Nair, S. A., Kurup, S. R. R., Nair, A. S., Baby, S. (2018). Citrus peels prevent cancer. Phytomedicine 50, 231–237. doi:10.1016/j.phymed.2017.08.011 CiT Saturn White Micro-ATX PC Gaming Case with 4 x 120mm Infinity ARGB Fans Included 1 x 4-Port Fan Hub Tempered Glass Side Panel Hauer-Jakli, M., Trankner, M. (2019). Critical leaf magnesium thresholds and the impact of magnesium on plant growth and photo-oxidative defense: a systematic review and meta-analysis from 70 years of research. Front. Plant Sci. 10. doi:10.3389/fpls.2019.00766 Hu, H., Fei, X., He, B., Luo, Y., Qi, Y., Wei, A. (2021). Integrated analysis of metabolome and transcriptome data for uncovering flavonoid components of zanthoxylum bungeanum maxim. leaves under drought stress. Front. Nutr. 8. doi:10.3389/fnut.2021.801244 Li, Y., Chen, Q. Y., Xie, X. D., Cai, Y., Li, J. F., Feng, Y. L., et al. (2020b). Integrated metabolomics and transcriptomics analyses reveal the molecular mechanisms underlying the accumulation of anthocyanins and other flavonoids in cowpea pod (Vigna unguiculata l.). J. Agric. Food Chem. 68, 9260–9275. doi:10.1021/acs.jafc.0c01851

Introduction

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 Wang, F., Chen, L., Chen, H. P., Chen, S. W., Liu, Y. P. (2019). Analysis of flavonoid metabolites in citrus peels (Citrus reticulata “Dahongpao”) using UPLC-ESI-MS/MS. Molecules 24. doi:10.3390/molecules24152680 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-x Du, H., Huang, Y., Tang, Y. (2010). Genetic and metabolic engineering of isoflavonoid biosynthesis. Appl. Microbiol. Biotechnol. 86, 1293–1312. doi:10.1007/s00253-010-2512-8

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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 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 Ferrer, J. L., Austin, M. B., Stewart, C., Jr., Noel, J. P. (2008). Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol. Biochem. 46, 356–370. doi:10.1016/j.plaphy.2007.12.009 Owens, D. K., Alerding, A. B., Crosby, K. C., Bandara, A. B., Westwood, J. H., Winkel, B. S. (2008). Functional analysis of a predicted flavonol synthase gene family in arabidopsis. Plant Physiol. 147, 1046–1061. doi:10.1104/pp.108.117457Zhang, Y., Li, Y., Li, W., Hu, Z., Yu, X., Tu, Y., et al. (2019). Metabolic and molecular analysis of nonuniform anthocyanin pigmentation in tomato fruit under high light. Hortic. Res. 6, 56. doi:10.1038/s41438-019-0138-2 CiT LT100 1 Litre USB3.0 Ultra-Thin Mini-ITX Computer Case With 120W Laptop Adpater CPU Cooler WIFI Antenna 5cm Included CiT Pro Android X Gaming Cube White Case with 3 x 120mm Infinity ARGB Fans 1 x 6-Port Fan Hub Tempered Glass Front and Side Panels Matsia, S., Tsave, O., Hatzidimitriou, A., Salifoglou, A. (2022). Chromium flavonoid complexation in an antioxidant capacity role. Int. J. Mol. Sci. 23. doi:10.3390/ijms23137171 Citation: Xiong B, Li Q, Yao J, Liu Z, Yang X, Yu X, Li Y, Liao L, Wang X, Deng H, Zhang M, Sun G and Wang Z (2023) Widely targeted metabolomic profiling combined with transcriptome analysis sheds light on flavonoid biosynthesis in sweet orange 'Newhall' (C. sinensis) under magnesium stress. Front. Plant Sci. 14:1182284. doi: 10.3389/fpls.2023.1182284