Abstract
One of the most important qualities of jujube fruit is its color. Chlorophyll, carotenoid, and anthocyanin all play important roles in the coloring of jujube fruit. However, few studies have focused on the pigment molecular mechanism. In the present study, jujube peels of ‘Sanbianhong’ in three growth stages were evaluated for their gene expression characteristics and gene regulation related to pigment formation using the transcriptome sequencing analysis. A total of 84.86 Gb of clean data were obtained in the analysis. In the FS1 vs. FS3, FS1 vs. FS5, and FS3 vs. FS5, 4,530, 11,012, and 9,072 differentially expressed genes (DEGs) were identified, respectively. The inter-group screening among the three comparisons yielded 1430 common DEGs. Among these DEGs, 27, 16, and 28 genes were enriched in chlorophyll, carotenoid, and anthocyanin metabolic pathways, respectively. Twelve genes were chosen at random, and the accuracy of the transcriptome data were confirmed using qRT-PCR. The molecular mechanism underlying the pigmentation of jujube fruit was elucidated at the transcriptome level, which would provide a scientific basis for the subsequent functional studies on the color-regulating genes of jujube fruits.
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The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol: FPB 38(11):833–847
Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15(5):266–274
Chen J, Tsim K (2020) A review of edible jujube, the Ziziphus jujuba fruit: a heath food supplement for anemia prevalence. Front Pharmacol 11:593655
Choi SH, Ahn JB, Kim HJ, Im NK, Kozukue N, Levin CE, Friedman M (2012) Changes in free amino acid, protein, and flavonoid content in jujube (Ziziphus jujube) fruit during eight stages of growth and antioxidative and cancer cell inhibitory effects by extracts. J Agric Food Chem 60(41):10245–10255
Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56(1):1–14
Feng Z, Gao Z, Jiao X, Shi J, Wang R (2020) Widely targeted metabolomic analysis of active compounds at different maturity stages of ‘Hupingzao’jujube. J Food Compos Anal 88:103417
Gao QH, Wu CS, Wang M (2013) The jujube (Ziziphus jujuba Mill.) fruit: a review of current knowledge of fruit composition and health benefits. J Agric Food Chem 61(14):3351–3363
Gu KD, Wang CK, Hu DG, Hao YJ (2019) How do anthocyanins paint our horticultural products? Sci Hortic 249:257–262
Guo M, Zhang Z, Li S, Lian Q, Fu P, He Y, Qiao J, Xu K, Liu L, Wu M, Du Z, Li S, Wang J, Shao P, Yu Q, Xu G, Li D, Wang Y, Tian S, Zhao J, Feng X, Li R, Jiang W, Zhao X (2021) Genomic analyses of diverse wild and cultivated accessions provide insights into the evolutionary history of jujube. Plant Biotechnol J 19(3):517–531
Kou X, Chen Q, Li X, Li M, Kan C, Chen B, Zhang Y, Xue Z (2015) Quantitative assessment of bioactive compounds and the antioxidant activity of 15 jujube cultivars. Food Chem 173:1037–1044
Landrum JT, Bone RA (2001) Lutein, zeaxanthin, and the macular pigment. Arch Biochem Biophys 385(1):28–40
Li Y (2017) The molecular mechanism research on the red pigment development of Zizyphus Jujuba Mill cv. Dongzao. Doctoral dissertation. Tianjin University, Tianjin
Li DK, Niu XW, Tian JB (2013) The Illustrated Germplasm Resources of Chinese. Agriculture Press, Beijing
Li S, Deng B, Tian S, Guo M, Liu H, Zhao X (2021) Metabolic and transcriptomic analyses reveal different metabolite biosynthesis profiles between leaf buds and mature leaves in Ziziphus jujuba Mill. Food Chem 347:129005
Liu MJ, Wang M (2009) Chinese jujube germsplasm resources. China Forestry Publishing House Press, Beijing
Liu MJ, Zhao J, Cai QL, Liu GC, Wang JR, Zhao ZH, Liu P, Dai L, Yan G, Wang WJ, Li XS, Chen Y, Sun YD, Liu ZG, Lin MJ, Xiao J, Chen YY, Li XF, Wu B, Ma Y, Jian JB, Yang W, Yuan Z, Sun XC, Wei YL, Yu LL, Zhang C, Liao SG, He RJ, Guang XM, Wang Z, Zhang YY, Luo LH (2014) The complex jujube genome provides insights into fruit tree biology. Nat Commun 5:5315
Liu M, Wang J, Wang L, Liu P, Zhao J, Zhao Z, Yao S, Stănică F, Liu Z, Wang L, Ao C, Dai L, Li X, Zhao X, Jia C (2020) The historical and current research progress on jujube-a superfruit for the future. Hortic Res 7:119
Liu H, Wang L, Liu H, Deng B, Li S, Zhao X (2022) Quantification and identification analysis of Ziziphus jujuba Mill. peel pigmentation at different developmental stages. Food Chem: X 16:100470
Lu Y, Bao T, Mo J, Ni J, Chen W (2021) Research advances in bioactive components and health benefits of jujube (Ziziphus jujuba Mill.) fruit. J Zhejiang Univ—Sci B 22(6):431–449
Miller R, Owens SJ, Rørslett B (2011) Plants and colour: flowers and pollination. Opt Laser Technol 43(2):282–294
Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid Metabolism in Plants. Mol Plant 8(1):68–82
Qing J, Dawei W, Jun Z, Yulan X, Bingqi S, Fan Z (2019) Genome-wide characterization and expression analyses of the MYB superfamily genes during developmental stages in Chinese jujube. PeerJ 7:e6353
Qu ZZ, Wang YY (1993) China fruit’s monograph-Chinese jujube volume. China Forestry Publishing House Press, Beijing
Rashwan AK, Karim N, Shishir MRI, Bao T, Lu Y, Chen W (2020) Jujube fruit: a potential nutritious fruit for the development of functional food products. J Funct Foods 75:104205
Reche J, Almansa MS, Hernández F, Amorós A, Legua P (2021) Physicochemical and antioxidant capacity of Jujube (Ziziphus jujuba Mill.) at different maturation stages. Agronomy 11(1):132
Rüdiger W (2002) Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth Res 74(2):187–193
Shi Q (2019) Molecuar mechanism of the formation of fruit pigment in jujube fruits. Doctoral dissertation. Northwest A & F University, Xianyang
Shi Q, Zhang Z, Su J, Zhou J, Li X (2018) Comparative analysis of pigments phenolics and antioxidant activity of Chinese jujube (Ziziphus jujuba Mill.) during fruit development. Molecules 23(8):1917
Shi Q, Du J, Zhu D, Li X, Li X (2020) Metabolomic and transcriptomic analyses of anthocyanin biosynthesis mechanisms in the color mutant Ziziphus jujuba cv. Tailihong. J Agric Food Chem 68(51):15186–15198
Takamiya KI, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5(10):426–431
Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9(3):248–255
Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J: Cell Mol Biol 54(4):733–749
Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20(3):327–341
Wojdyło A, Carbonell-Barrachina ÁA, Legua P, Hernández F (2016) Phenolic composition, ascorbic acid content, and antioxidant capacity of Spanish jujube (Ziziphus jujube Mill.) fruits. Food Chem 201:307–314
Xue X, Zhao A, Wang Y, Ren H, Li Y, Li D, Du J (2022) Metabolomics-based analysis of flavonoid metabolites in Chinese jujube and sour jujube fruits from different harvest periods. J Food Sci 87(9):3752–3765
Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Hortic Res 2:15036
Zhang Q (2010) Identification of pigments from jujube fruit skin. J Anhui Agric Sci 2013(1):47–70
Zhang Q (2020) Analysis of peel structure and components related to pigment accumulation during jujube coloring. Doctoral dissertation. Hebei agricultural University, Baoding
Zhang H, Jiang L, Ye S, Ye Y, Ren F (2010) Systematic evaluation of antioxidant capacities of the ethanolic extract of different tissues of jujube (Ziziphus jujuba Mill.) from China. Food Chem Toxicol: Int J Publ Br Ind Biol Res Assoc 48(6):1461–1465
Zhang Q, Wang L, Liu Z, Zhao Z, Zhao J, Wang Z, Zhou G, Liu P, Liu M (2020) Transcriptome and metabolome profiling unveil the mechanisms of Ziziphus jujuba Mill. peel coloration. Food Chem 312:125903
Zhang Q, Wang L, Wang Z, Liu Z, Zhao Z, Zhou G, Liu M, Liu P (2020) Variations of the nutritional composition of jujube fruit (Ziziphus jujuba Mill) during maturation stages. Int J Food Prop 23(1):1066–1081
Funding
This work was supported by National Natural Science Foundation of China (Grant Number. 32101565), and Henan Provincial Science and Technology Research Project (Grant Number. 212102110183).
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SL conducted most of the experiments, including sample collection, transcriptomics data analysis and qRT-PCR analysis. YW performed the chlorophyll, carotenoid, and anthocyanin pathway analysis. YS and SZ participated in qRT-PCR analysis. HL performed the correlation analysis between metabolites and gene expression levels. SL designed and supervised the study and wrote the first draft of the manuscript.
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Li, S., Wang, Y., Shen, Y. et al. Transcriptome Characterization of Pigment-Related Genes in Jujube (Ziziphus Jujuba Mill.) Peel at Different Growth Stages. Biochem Genet 61, 2425–2442 (2023). https://doi.org/10.1007/s10528-023-10382-0
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DOI: https://doi.org/10.1007/s10528-023-10382-0