Screening of Ziziphus jujuba‘Hupingzao’Fruit Coloring Substances and Their Related Genes

doi:10.16420/j.issn.0513-353x.2023-0527

Acta Horticulturae Sinica ›› 2024, Vol. 51 ›› Issue (8): 1728-1742.doi: 10.16420/j.issn.0513-353x.2023-0527

• Genetic & Breeding·Germplasm Resources·Molecular Biology • Previous Articles Next Articles

Screening of Ziziphus jujuba‘Hupingzao’Fruit Coloring Substances and Their Related Genes

LI Jie^*(), WU Chao, JIA Xiangqian, WANG Juan

College of Forestry Shanxi Agricultural University，Taigu，Shanxi 030801，China

Received:2023-07-26 Revised:2020-10-23 Online:2024-08-25 Published:2024-08-21
Contact: LI Jie

Abstract

Abstract:

The white ripening，semi-red and whole red fruits of Ziziphus jujuba‘Hupingzao’as materials，the contents of the main pigment substances in the peel were determined and transcriptome sequencing was carried out to elaborate the changes of coloring genes in the peel of jujube at the molecular level. The results showed that after the white ripening period，the anthocyanin content of jujube peel began to decrease significantly. In the three periods，the flavonoid content of jujube peel decreased significantly. The chlorophyll content did not change much from the white maturity stage to the semi-red stage，and decreased significantly at the full red stage. The content of carotenoids was relatively stable in the veraison stage. Flavonoids，anthocyanins，carotenoids and chlorophyll are the coloring substances of jujube peel，and the anthocyanins are divided into six types：delphinidin，cyanidin，petunidin，malvidin，peonidin and pelargonidin. According to the GO and KEGG enrichment analysis in transcriptome sequencing，the number of differential genes in flavonoids，anthocyanins，flavonoids and flavonols，carotenoids and porphyrin metabolic pathways were 35，22，6，30 and 38，respectively. Among them，the white anthocyanidin reductase gene（LOC107429483），transcription factor gene MYC2（LOC107430586）and dihydroflavonol 4-reductase gene（LOC107420289）played a major role in the coloring of jujube peel，and β-carotene hydroxylase gene（LOC107414761）was the key gene affecting carotenoid synthesis. The chloroplast A oxygenase gene（LOC107410684）in porphyrin metabolism is a key gene affecting total chlorophyll content.

Key words: Ziziphus jujuba, coloring, RNA-Seq, flavonoids, anthocyanins

LI Jie, WU Chao, JIA Xiangqian, WANG Juan. Screening of Ziziphus jujuba‘Hupingzao’Fruit Coloring Substances and Their Related Genes[J]. Acta Horticulturae Sinica, 2024, 51(8): 1728-1742.

Figures/Tables 13

Fig. 1 The white ripening（left），semi-red（middle）and whole red（right）fruits of Ziziphus jujuba‘Hupingzao’

Fig. 2 Changes in the contents of anthocyanins and flavonoids in the peel of Ziziphus jujuba‘Hupingzao’in three periods Different lowercase letters indicated significant differences in the same index in different periods（P < 0.05）.The same below.

Fig. 3 Changes in chlorophyll and carotenoid contents in the peel of Ziziphus jujuba‘Hupingzao’in three stages

Table 1 The content of various flavonoid substances in three kinds of Ziziphus jujuba‘Hupingzao’fruit

化合物种类 Compound type	含量/（ng · mL^-1） Content	化合物种类 Compound type	含量/（ng · mL^-1） Content
矢车菊素双葡萄糖苷Cyanidin 3,5-diglucoside	—	天竺葵色素Pelargonidin 锦葵色素Malvidin	6.566 15.392
矢车菊素半乳糖苷Cyanidin 3-galactoside	2.809	芍药色素Peonidin	7.794
飞燕草素Delphinidin	—	芦丁（芸香苷）Rutin	8.714
原花色素B4 Procyanidin B4	5.720	木犀草素Luteolin	136.234
矢车菊素Cyanidin	21.938	槲皮素Quercetin	44.376
双聚原矢车菊甘元Procyanidin B2	7.952	异鼠李素Isorhamnetin	32.522
矮牵牛色素Petunidin	23.033	山奈酚Kaempferol	31.923

Table 2 Overview of sample sequencing data

时期 Stage	样本 Sample	原始碱基数 Total bases	样本碱基总数/Gb Total giga bases	有效序列数 Total reads	Q20/%	Q30/%	比对率 Overall mapping rate
白熟期White ripening	1	6 469 880 608	6.47	44 889 082	97.9148	93.7792	0.946
	2	5 857 844 975	5.86	40 652 034	98.0241	94.0759	0.944
	3	6 166 062 009	6.17	42 803 420	97.8849	93.6980	0.944
半红期Semi-red	1	5 757 384 355	5.76	39 806 298	98.3328	94.8011	0.952
	2	6 114 634 623	6.11	42 321 102	98.0420	94.0131	0.951
	3	6 452 091 835	6.45	44 670 074	98.1427	94.3092	0.938
全红期Whole-red	1	5 731 716 448	5.73	39 656 256	98.1848	94.4039	0.953
	2	5 676 944 756	5.68	39 237 730	98.2798	94.6434	0.952
	3	6 040 803 819	6.04	41 780 350	98.2849	94.6781	0.954

Fig. 4 The number of differentially expressed genes in the Ziziphus jujuba‘Hupingzao’in the three stages BSQ：White ripening；BHQ：Semi-red；QHQ：Whole red.

Fig. 5 Three stages of GO annotation of Ziziphus jujuba‘Hupingzao’DEGs

Fig. 6 Map of KEGG concentration and distribution point of different genes in pericarp of Ziziphus jujuba‘Hupingzao’at white ripening stage and semi-red stage

Fig. 7 Map of KEGG concentration and distribution point of pericarp differential gene in semi-red stage and whole red stage of Ziziphus jujuba‘Hupingzao’

Fig. 8 Map of KEGG concentration and distribution point of different genes in pericarp of Ziziphus jujuba‘Hupingzao’ during white ripening stage and whole red stage

Fig. 9 Heat map of differentially expressed genes in metabolic pathways related to Ziziphus jujuba‘Hupingzao’peel coloring at different stages enriched by KEGG

Fig. 10 Cluster analysis of differentially expressed genes in Ziziphus jujuba‘Hupingzao’ peel coloring at different stages of KEGG enrichment

Fig. 11 Diagram of anthocyanin synthesis pathway Three color blocks from left to right represent the expression of white ripe stage，semi-red stage and whole red stage.

References 32

[1]	An X H, Tian Y, Chen K Q, Liu X J, Liu D D, Xie X B, Cheng C G, Cong P H, Hao Y J. 2015. MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant & Cell Physiology, 56 (4):650-662.
[2]	Azuma A, Kobayashi S, Mitani N, Shiraishi M, Yamada M, Ueno T, Kono A, Yakushiji H, Koshita Y. 2008. Genomic and genetic analysis of Myb-related genes that regulate anthocyanin biosynthesis in grape berry skin. Theoretical and Applied Genetics,117:1009-1019.
[3]	Cao Z H, Zhang S Z, Wang R K, Zhang R F, Hao Y J. 2013. Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE,8:e69955.
[4]	Cesa S, Carradori S, Bellagamba G, Locatelli M, Casadei M A, Masci A, Paolicelli P. 2017. Evaluation of processing effects on anthocyanin content and colour modifications of blueberry(Vaccinium spp.) extracts:comparison between HPLC-DAD and CIELAB analyses. Food Chemistry,232:114-123.
[5]	Chang Shimin, Sheng Jiping, Shen Lin. 2004. Extraction and analysis of pigments from Dongzao jujube. Storage and Process,(5):18-20. (in Chinese)
	常世敏, 生吉萍, 申琳. 2004. 冬枣果皮红色素提取及其性质的分析研究. 保鲜与加工,(5):18-20.
[6]	Chi Xin, Wang Xinyue, Song Laiqing, Jiang Zhongwu, Du Xiaoyun. 2019. Progress in the study of apple peel coloration. Yantai Fruits, 147 (3):4-6. (in Chinese)
	迟馨, 王心悦, 宋来庆, 姜中武, 杜晓云. 2019. 苹果果皮着色的研究进展. 烟台果树, 147 (3):4-6.
[7]	Chikako H, Shigeki M. 2018. Anthocyanin biosynthesis in apple fruit. The Horticulture Journal, 87 (3):305-314.
[8]	Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde J P, Mérillon J M, Hamdi S. 2006. Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiology, 140 (2):499-511. doi: 10.1104/pp.105.067231 pmid: 16384897
[9]	Dzhanfezova T, Barba E G, Müller R, Joernsgaard B, Hegelund J N, Madsen B, Larsen D H, Vega M V, Toldam A T B. 2020. Anthocyanin profile,antioxidant activity and total phenolic content of a strawberry(Fragaria × ananassa Duch)genetic resource collection. Food Bioscience,36:100620.
[10]	Feng S Q, Wang Y L, Song Y, Xu Y T, Chen X S. 2010. Anthocyanin biosynthesis in pears is regulated by a R2R3-MYB transcription factor PyMYB10. Planta,232:245-255.
[11]	Gu K D, Wang C K, Hu D G, Hao Y J. 2019. How do anthocyanins paint our horticultural products. Scientia Horticulturae,249:257-262.
[12]	Li Jie. 2019. Study on the mechanism of plant growth regulator on fruit coloring of Ziziphus jujuba Mill.[Ph. D. Dissertation]. Taigu: Shanxi Agricultural University. (in Chinese)
	李洁. 2019. 生长调节剂对壶瓶枣(Ziziphus jujuba‘Hupingzao’)果实转色调控机制研究[博士论文]. 太谷: 山西农业大学.
[13]	Li S P, Wang Y, Shen Y Y, Zheng S P, Liu H X. 2023. Transcriptome characterization of pigment-related genes in jujube(Ziziphus jujuba Mill.) peel at different growth stages. Biochemical Genetics, 61 (6):2425-2442.
[14]	Li Xiao, Zhao Wenen, Tiao Wutao, Shi Guoqing, Guo Penghui, Hu Liqiang. 2009. The research of the separation of the red pigment in juiube rind and analysis of the components. Tianjin Chemical Industry, 23 (3):37-39. (in Chinese)
	李晓, 赵文恩, 田武韬, 时国庆, 郭朋辉, 胡利强. 2009. 枣皮红色素的成分分离分析研究. 天津化工, 23 (3):37-39.
[15]	Lichtenthaler H K, Buschmann C. 2001. Chlorophylls and carotenoids:measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry, 1,F4.3.1-F4.3.8.
[16]	Liu H X, Wang L F, Liu H, Deng B L, Li S P. 2022. Quantifcation and identifcation analysis of Ziziphus jujuba Mill. peel pigmentation at diferent developmental stages. Food Chemistry:X,16:100470.
[17]	Ma G, Zhang L, Yung Y W, Sato Y, Furuya T, Yahata M, Yamawaki K, Kato M. 2018. Accumulation of carotenoids in a novel citrus cultivar ‘Seinannohikari’during the fruit maturation. Plant Physiology and Biochemistry, 129 (7):349-356.
[18]	Miao Lijun, Liu Mengjun, Peng Hongli, Wang Jing, Qin Ziyu, Zou Lei, Zhang Ying. 2008. Analysis on total flavonoid content in jujube fruit. Anhui Agricultural Sciences,(22):9460-9461. (in Chinese)
	苗利军, 刘孟军, 彭红丽, 王静, 秦子禹, 邹磊, 张颖. 2008. 枣果中总黄酮含量分析. 安徽农业科学,(22):9460-9461.
[19]	Miller R, Owens S J, Rørslett B. 2011. Plants and colour:fowers and pollination. Optics & Laser Technology, 43 (2):282-294.
[20]	Reche J, Almansa M S, Hernández F, Amorós A, Legua P. 2021. Physicochemical and antioxidant capacity of jujube(Ziziphus jujuba Mill.) at diferent maturation stages. Agronomy, 11 (1):132.
[21]	Ren Zhengkai, Huang Shaopeng, Feng Shun, Kou Jingjing, Wu Fan, Li Cuiling, Li Maofu. 2023. Correlation analysis between coloration and key enzyme activities of avocado peel. Molecular Plant Breeding, https://kns.cnki.net/kcms/detail/46.1068.S.20230516.1424.020.html. in Chinese)
	任正恺, 黄少鹏, 冯顺, 寇静静, 吴凡, 李翠玲, 李茂富. 2023. 油梨果皮着色与关键酶活性相关性分析. 分子植物育种, https://kns.cnki.net/kcms/detail/46.1068.S.20230516.1424.020.html.
[22]	Shi Q Q, Zhang Q, Su J J, Zhou J, Li X G. 2018. Comparative analysis of pigments phenolics and antioxidant activity of Chinese jujube(Ziziphus jujuba Mill.) during fruit development. Molecules, 23 (8):1917.
[23]	Shi Q Q, Du J T, Zhu D J, Li X, Li X G. 2020. Metabolomic and transcriptomic analyses of anthocyanin biosynthesis mechanisms in the color mutant Ziziphus jujuba cv. Tailihong. Journal of Agricultural and Food Chemistry, 68 (51):15186-15198.
[24]	Shi Qianqian. 2019. Molecuar mechanism of the formation of fruit pigment in jujube fruits[Ph. D. Dissertation]. Yangling: Northwest A & F University. (in Chinese)
	石倩倩. 2019. 枣果实色泽性状形成的分子机制研究[博士论文]. 杨凌: 西北农林科技大学.
[25]	Tanaka A, Tanaka R. 2006. Chlorophyll metabolism. Current Opinion in Plant Biology, 9 (3):248-255. doi: 10.1016/j.pbi.2006.03.011 pmid: 16603411
[26]	Tanaka Y, Sasaki N, Ohmiya A. 2008. Biosynthesis of plant pigments:anthocyanins,betalains and carotenoids. The Plant Journal:for Cell and Molecular Biology, 54 (4):733-749.
[27]	Xu Haifeng, Wang Zhongtang, Chen Xin, Liu Zhiguo, Wang Lihu, Liu Ping, Liu Mengjun, Zhang Qiong. 2022. The analyses of target metabolomics in flavonoid and its potential MYB regulation factors during coloring period of winter jujube. Acta Horticultural Sinica, 49 (8):1761-1771. (in Chinese)
	许海峰, 王中堂, 陈新, 刘志国, 王利虎, 刘平, 刘孟军, 张琼. 2022. 冬枣果皮着色相关类黄酮靶向代谢组学及潜在MYB转录因子分析. 园艺学报, 49 (8):1761-1771. doi: 10.16420/j.issn.0513-353x.2021-0326
[28]	Xue X F, Zhao A L, Wang Y K, Ren H Y, Li Y, Li D K, Du J J. 2022. Metabolomics-based analysis of favonoid metabolites in Chinese jujube and sour jujube fruits from diferent harvest periods. Journal of Food Science, 87 (9):3752-3765.
[29]	You Feng, Huang Lixin, Zhang Caihong, Xie Pujun, Zhang Yaolei. 2013. Preliminary study on spectrums and structure properties of pigments from Ziziphus jujube peel. Science and Technology of Food Industry, 34 (13):99-102,105. (in Chinese)
	游凤, 黄立新, 张彩虹, 谢普军, 张耀雷. 2013. 冬枣皮色素各组分光谱性质及结构的初步研究. 食品工业科技, 34 (13):99-102,105.
[30]	Yuan H, Zhang J X, Nageswaran D, Li L. 2015. Preliminary study on spectrums and structure properties of pigments from Ziziphus jujube peel. Horticulture Research,2:15036.
[31]	Zhao Jing, Li Hanhan, Qiao Wen, Piao Changshan, Yang Changqing. 2021. Comparison of method for determination of anthocyanins in black chokeberry. Food Science, 42 (18):212-217. (in Chinese) doi: 10.7506/spkx1002-6630-20200901-003
	赵婧, 李涵涵, 千文, 朴昌善, 杨长青. 2021. 黑果腺肋花楸果中总花色苷含量测定方法的比较. 食品科学, 42 (18):212-217.
[32]	Zhang Q, Wang L L, Liu Z G, Zhao Z H, Zhao J, Wang Z T, Zhou G F, Liu P, Liu M J. 2020. Transcriptome and metabolome profiling unveil the mechanisms of Ziziphus jujuba Mill. peel coloration. Food Chemistry,312:125903.

Screening of Ziziphus jujuba‘Hupingzao’Fruit Coloring Substances and Their Related Genes

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