Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (11): 3296-3311    DOI: 10.1016/j.jia.2023.09.029
Special Issue: 园艺作物品质提升与逆境适应性Horticulture——Quality Improvement & Stress adaptation
Special Focus: Germplasm and Molecular Breeding in Horticultural Crops Advanced Online Publication | Current Issue | Archive | Adv Search |
Blue light induces leaf color change by modulating carotenoid metabolites in orange-head Chinese cabbage (Brassica rapa L. ssp. pekinensis)

ZHANG Rui-xing1, ZHANG Ni-nan1, WANG Ya-xiu1, Khan ABID2, MA Shuai1, BAI Xue1, ZENG Qi1, PAN Qi-ming1, LI Bao-hua1#, ZHANG Lu-gang1#

1 State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, P.R.China
2 Department of Horticulture, The University of Haripur, Haripur 22620, Pakistan
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

类胡萝卜素参与植物叶色的形成以及光系统的光保护。在这项研究中,我们发现蓝光会显着上调橙色大白菜内叶中的总类胡萝卜素。此外,转录组学分析显示,蓝光处理诱导类胡萝卜素代谢途径上游的光合作用(BrHY5-2BrCOP1BrDET1)和MEP(甲基赤藓糖醇 4-磷酸)(BrGGPSBrDXSBrHDR)途径中的基因上调。类胡萝卜素代谢组学分析显示,蓝光处理后几种橙色和红色类胡萝卜素(番茄红素、玉米黄质、β-胡萝卜素、叶黄素和β-隐黄质)的积累有助于叶片橙色的加深,表明短期蓝光治疗可用于促进有益营养的积累。光信号基因 BrHY5-2 参与了橙色大白菜中类胡萝卜素生物合成的蓝光诱导转录调控。BrHY5-2在拟南芥中的过表达显著增加了总类胡萝卜素含量和对蓝光的敏感性。上述发现揭示了蓝光诱导橙色大白菜品系中类胡萝卜素合成和积累的新见解,并提供了提高蔬菜营养价值的新方法。



Abstract  

Carotenoids are involved in the formation of plant leaf color as well as photosystem photoprotection.  This study showed that blue light significantly induced up-regulation of the total carotenoid content in the inner leaves of orange-head Chinese cabbage (OHCC).  Furthermore, the transcriptomic analysis revealed that blue light treatment induced up-regulation of genes in photosynthesis (BrHY5-2, BrCOP1 and BrDET1) and the methylerythritol 4-phosphate pathways (BrGGPS, BrDXS and BrHDR) upstream of the carotenoid metabolic pathway.  Carotenoid metabolomic analysis revealed that the accumulation of several orange and red carotenoids (lycopene, zeaxanthin, β-carotene, lutein, and β-cryptoxanthin) after blue light treatment contributed to the deepening of the leaf coloration, suggesting that short-term blue light treatment could be used to boost nutritional quality.  The light signal gene BrHY5-2 participated in the blue light-induced transcriptional regulation of carotenoid biosynthesis in OHCC.  Overexpression of BrHY5-2 in Arabidopsis significantly increased the total carotenoid content and the sensitivity to blue light.  The above findings revealed new insights about blue-light-induced carotenoid synthesis and accumulation in OHCC lines.  They suggested a new engineering approach to increase the nutritional value of vegetables.

Keywords:  orange heading Chinese cabbage (OHCC)       carotenoid       nutrition       blue LED light       secondary metabolite       transcriptome  
Received: 22 January 2023   Accepted: 19 May 2023
Fund: This work was supported by the National Key Research and Development Program of China (2017YFD0101802 and 2016YFD0101701), the Key Research and Development Program of Yangling Seed Innovative Center, China (Ylzy-sc-04) and the Key Research and Development Program of Shaanxi Province, China (2023-YBNY-078).
About author:  ZHANG Rui-xing, E-mail: xingqing@nwafu.edu.cn; #Correspondence LI Bao-hua, E-mail: baohuali@nwafu.edu.cn; ZHANG Lu-gang, E-mail: lugangzh@nwafu.edu.cn

Cite this article: 

ZHANG Rui-xing, ZHANG Ni-nan, WANG Ya-xiu, Khan ABID, MA Shuai, BAI Xue, ZENG Qi, PAN Qi-ming, LI Bao-hua, ZHANG Lu-gang. 2023. Blue light induces leaf color change by modulating carotenoid metabolites in orange-head Chinese cabbage (Brassica rapa L. ssp. pekinensis). Journal of Integrative Agriculture, 22(11): 3296-3311.

Atuna R A, Achaglinkame M A, Accorley T A S, Amagloh F K. 2021. Cassava orange-fleshed sweetpotato composite Gari: A potential source of dietary vitamin A. Frontiers in Nutrition8, 646051–646051.

Chenge-Espinosa M, Cordoba E, Romero-Guido C, Toledo-Ortiz G, Leon P. 2018. Shedding light on the methylerythritol phosphate (MEP)-pathway: Long hypocotyl 5 (HY5)/phytochrome-interacting factors (PIFs) transcription factors modulating key limiting steps. Plant Journal96, 828–841.

Clough S J, Bent A F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thalianaPlant Journal16, 735–743.

Cordoba E, Salmi M, León P. 2009. Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. Journal of Experimental Botany60, 2933–2943.

Enfissi E M, Nogueira M, D’Ambrosio C, Stigliani A L, Giorio G, Misawa N, Fraser P D. 2019. The road to astaxanthin production in tomato fruit reveals plastid and metabolic adaptation resulting in an unintended high lycopene genotype with delayed over-ripening properties. Plant Biotechnology Journal17, 1501–1513.

Esteban R, Moran J F, Becerril J M, García-Plazaola J I. 2015. Versatility of carotenoids: An integrated view on diversity, evolution, functional roles and environmental interactions. Environmental and Experimental Botany119, 63–75.

Estévez J M, Cantero A, Romero C, Kawaide H, Jiménez L F, Kuzuyama T, Seto H, Kamiya Y, León P. 2000. Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D -erythritol-4-phosphate pathway in Arabidopsis. Plant Physiology124, 95–104.

Jahns P, Holzwarth A R. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta (BBA) - Bioenergetics1817, 182–193.

Kirk H, Cheng D, Choi Y H, Vrieling K, Klinkhamer P G L. 2012. Transgressive segregation of primary and secondary metabolites in F2 hybrids between Jacobaea aquatica and JvulgarisMetabolomics8, 211–219.

Klee H J, Giovannoni J J. 2011. Genetics and control of tomato fruit ripening and quality attributes. Annual Review of Genetics45, 41–59.

Kopsell D A, Sams C E. 2013. Increases in shoot tissue pigments, glucosinolates, and mineral elements in sprouting broccoli after exposure to short-duration blue light from light emitting diodes. Journal of the American Society for Horticultural Science138, 31–37.

Kopsell D A, Sams C E, Barickman T C, Morrow R C. 2014. Sprouting broccoli accumulate higher concentrations of nutritionally important metabolites under narrow-band light-emitting diode lighting. Journal of the American Society for Horticultural Science139, 469–477.

Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics9, 1–13.

Larkin R M, Ruckle M E. 2008. Integration of light and plastid signals. Current Opinion in Plant Biology11, 593–599.

Lewis E R, Nogueira M, Enfissi E M A, Fraser P D. 2021. The esterification of xanthophylls in Solanum lycopersicum (tomato) chromoplasts; the role of a non-specific acyltransferase. Phytochemistry191, 112912.

Li J, Lian X, Ye C, Wang L. 2019. Analysis of flower colorv ariations at different developmental stages in two honeysuckle (Lonicera Japonica Thunb.) cultivars. HortScience54, 779–782.

Lightenthaler H. 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology148, 350–382.

Liu Y, Lv J, Liu Z, Wang J, Yang B, Chen W, Ou L, Dai X, Zhang Z, Zou X. 2020. Integrative analysis of metabolome and transcriptome reveals the mechanism of color formation in pepper fruit (Capsicum annuum L.). Food Chemistry306, 125629.

Liu Y, Roof S, Ye Z, Barry C, Van Tuinen A, Vrebalov J, Bowler C, Giovannoni J. 2004. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proceedings of the National Academy of Sciences of the United States of America101, 9897–9902.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods25, 402–408.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology15, 550.

Ma S. 2020. Analysis of carotenoid accumulation characteristics and combining ability of inbred line in orange head Chinese cabbage. MSc thesis, Northwest A&F University, China. (in Chinese)

Marty I, Bureau S, Sarkissian G, Gouble B, Audergon J, Albagnac G. 2005. Ethylene regulation of carotenoid accumulation and carotenogenic gene expression in colour-contrasted apricot varieties (Prunus armeniaca). Journal of Experimental Botany56, 1877–1886.

Matsuura H, Watanabe M M, Kaya K. 2012. Echinenone production of a dark red-coloured strain of Botryococcus brauniiJournal of Applied Phycology24, 973–977.

Park C H, Park S Y, Park Y J, Kim J K, Park S U. 2020. Metabolite profiling and comparative analysis of secondary metabolites in Chinese cabbage, radish, and hybrid xBrassicoraphanusJournal of Agricultural and Food Chemistry68, 13711–13719.

Park C H, Yeo H J, Park S Y, Kim J K, Park S U. 2019. Comparative phytochemical analyses and metabolic profiling of different phenotypes of Chinese cabbage (Brassica rapa ssp. pekinensis). Foods8, 587.

Pola W, Sugaya S, Photchanachai S. 2019. Color development and phytochemical changes in mature green chili (Capsicum annuum L.) exposed to red and blue light-emitting diodes. Journal of Agricultural and Food Chemistry68, 59–66.

Ramel F, Ksas B, Akkari E, Mialoundama A S, Monnet F, Krieger-Liszkay A, Ravanat J L, Mueller M J, Bouvier F, Havaux M. 2013. Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet oxygen. The Plant Cell25, 1445–1462.

Rodriguez-Concepcion M, Avalos J, Bonet M L, Boronat A, Gomez-Gomez L, Hornero-Mendez D, Limon M C, Meléndez-Martínez A J, Olmedilla-Alonso B, Palou A. 2018. A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health. Progress in Lipid Research70, 62–93.

Schöttler M A, Tóth S Z. 2014. Photosynthetic complex stoichiometry dynamics in higher plants: Environmental acclimation and photosynthetic flux control. Frontiers in Plant Science5, 188.

Seetang-Nun Y, Sharkey T D, Suvachittanont W. 2008. Molecular cloning and characterization of two cDNAs encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase from Hevea brasiliensisJournal of Plant Physiology165, 991–1002.

Su T, Yu S, Zhang J W F, Yu Y, Zhang D, Zhao X, Wang W. 2015. Loss of function of the carotenoid isomerase gene BrCRTISO confers orange color to the inner leaves of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Molecular Biology Reporter33, 648–659.

Sumiasih I H, Poerwanto R, Efendi D, Agusta A, Yuliani S. 2018. β-Cryptoxanthin and zeaxanthin pigments accumulation to induce orange color on citrus fruits. In: Institute of Physics Conference SeriesMaterials Science and Engineering. Institute of Physics Publishing, England and Wales. 012074.

Toledo-Ortiz G, Huq E, Rodríguez-Concepción M. 2010. Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proceedings of the National Academy of Sciences of the United States of America107, 11626–11631.

Toledo-Ortiz G, Johansson H, Lee K P, Bou-Torrent J, Stewart K, Steel G, Rodríguez-Concepción M, Halliday K J. 2014. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genetics10, e1004416.

Watanabe M, Musumi K, Ayugase J. 2011. Carotenoid pigment composition, polyphenol content, and antioxidant activities of extracts from orange-colored Chinese cabbage. LWT-Food Science and Technology44, 1971–1975.

Wilson M F. 1985. A rapid method for the separation and quantification of simple phenolic acids in plant material using high-performance liquid chromatography. Journal of Chromatography (A), 346, 440–445.

Xiao Y, Chu L, Zhang Y, Bian Y, Xiao J, Xu D. 2022. HY5: A pivotal regulator of light-dependent development in higher plants. Frontiers in Plant Science12, 989.

Xie B, Wei J, Zhang Y, Song S, Wei S, Sun G, Hao Y, Liu H. 2019. Supplemental blue and red light promote lycopene synthesis in tomato fruits. Journal of Integrative Agriculture18, 590–598.

Zhang J, Li H, Zhang M, Hui M, Wang Q, Li L, Zhang L. 2013. Fine mapping and identification of candidate Br-or gene controlling orange head of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Molecular Breeding32, 799–805.

Zhang J, Yuan H, Fei Z, Pogson B J, Zhang L, Li L. 2015. Molecular characterization and transcriptome analysis of orange head Chinese cabbage (Brassica rapa L. ssp. pekinensis). Planta241, 1381–1394.

Zhang L, Ma G, Kato M, Yamawaki K, Takagi T, Kiriiwa Y, Ikoma Y, Matsumoto H, Yoshioka T, Nesumi H. 2012. Regulation of carotenoid accumulation and the expression of carotenoid metabolic genes in citrus juice sacs in vitroJournal of Experimental Botany63, 871–886.

Zhang L, Ma G, Yamawaki K, Ikoma Y, Matsumoto H, Yoshioka T, Ohta S, Kato M. 2015. Effect of blue LED light intensity on carotenoid accumulation in citrus juice sacs. Journal of Plant Physiology188, 58–63.

Zhou W, Niu Y, Ding X, Zhao S, Li Y, Fan G, Zhang S, Liao K. 2020. Analysis of carotenoid content and diversity in apricots (Prunus armeniaca L.) grown in China. Food Chemistry330, 127223.

[1] Xuehao Zhang, Qiuling Zheng, Yongjiang Hao, Yingying Zhang, Weijie Gu, Zhihao Deng, Penghui Zhou, Yulin Fang, Keqin Chen, Kekun Zhang. Physiology and transcriptome profiling reveal the drought tolerance of five grape varieties under high temperatures[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3055-3072.
[2] Shan Wang, Kailin Shi, Yufan Xiao, Wei Ma, Yiguo Hong, Daling Feng, Jianjun Zhao. The circadian clock shapes diurnal gene expression patterns linked to glucose metabolic processes in Chinese cabbage[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2155-2170.
[3] Berhane S. Gebregziabher, Shengrui Zhang, Jing Li, Bin Li, Junming Sun. Identification of genomic regions and candidate genes underlying carotenoid accumulation in soybean using next-generation sequen-cing based bulk segregant analysis[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2063-2079.
[4] Xinyi Mao, Xuan Zhao, Zhi Luo, Ao He, Meng Yang, Mengjun Liu, Jin Zhao, Ping Liu. Transcriptome-based analysis of lignin accumulation in the regulation of fruit stone development and endocarp hardening in Chinese jujube[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2217-2228.
[5] Teame Gereziher Mehari, Marijana Skorić, Hui Fang, Kai Wang, Fang Liu, Tesfay Araya, Branislav Šiler, Dengbing Yao, Baohua Wang. Insights into the role of GhCYP and GhTPS in the gossypol biosynthesis pathway via a multiomics and functional-based approach in cotton[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1671-1687.
[6] Congrui Sun, Runze Wang, Jiaming Li, Xiaolong Li, Bobo Song, David Edwards, Jun Wu. Pan-transcriptome analysis provides insights into resistance and fruit quality breeding of pear (Pyrus pyrifolia)[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1813-1830.
[7] Jin Wang, Minghua Wei, Haiyan Wang, Changjuan Mo, Yingchun Zhu, Qiusheng Kong. A time-course transcriptome reveals the response of watermelon to low-temperature stress[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1786-1799.
[8] Bo Pang, Lirong Zhao, Xingxing Ma, Jiangtao Hong, Ziyin Du, Xiaodan Wang. Vegetation patches modify the acquisition of nitrogen by plants and microorganisms in a degraded alpine steppe[J]. >Journal of Integrative Agriculture, 2025, 24(3): 925-935.
[9] Xiaochun Wei, Yuanlin Zhang, Yanyan Zhao, Weiwei Chen, Ujjal Kumar Nath, Shuangjuan Yang, Henan Su, Zhiyong Wang, Wenjing Zhang, Baoming Tian, Fang Wei, Yuxiang Yuan, Xiaowei Zhang. Mitotic pollen abnormalities are linked to Ogura cytoplasmic male sterility in Chinese cabbage (Brassica rapa L. ssp. pekinensis)[J]. >Journal of Integrative Agriculture, 2025, 24(3): 1092-1107.
[10] Bowen Xu, Tingting Xu, Wenli Ding, Shucheng Huang. Diagnosis of leg diseases in broiler chickens: A retrospective review[J]. >Journal of Integrative Agriculture, 2025, 24(3): 984-1000.
[11] Yonghui Fan, Yue Zhang, Yu Tang, Biao Xie, Wei He, Guoji Cui, Jinhao Yang, Wenjing Zhang, Shangyu Ma, Chuanxi Ma, Haipeng Zhang, Zhenglai Huang.
Response of wheat to winter night warming based on physiological and transcriptome analyses
[J]. >Journal of Integrative Agriculture, 2025, 24(3): 1044-1064.
[12] Yiying Li, Yuanyuan Hu, Bei Wang, Mengyao Lang, Shutang Zhou, Zhongxia Wu. Transcriptome-based analysis reveals chromatin remodeling in post-adult eclosion reconstruction of the insect fat body[J]. >Journal of Integrative Agriculture, 2025, 24(2): 668-679.
[13] Yang Wang, Chunhua Mu, Xiangdong Li, Canxing Duan, Jianjun Wang, Xin Lu, Wangshu Li, Zhennan Xu, Shufeng Sun, Ao Zhang, Zhiqiang Zhou, Shenghui Wen, Zhuanfang Hao, Jienan Han, Jianzhou Qu, Wanli Du, Fenghai Li, Jianfeng Weng. A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize[J]. >Journal of Integrative Agriculture, 2025, 24(2): 453-466.
[14] Dongming Liu, Jinfang Liang, Quanquan Liu, Yaxin Chen, Shixiang Duan, Dongling Sun, Huayu Zhu, Junling Dou, Huanhuan Niu, Sen Yang, Shouru Sun, Jianbin Hu, Luming Yang. The pseudo-type response regulator gene Clsc regulates rind stripe coloration in watermelon[J]. >Journal of Integrative Agriculture, 2025, 24(1): 147-160.
[15] Lijiao Ge, Weihao Miao, Kuolin Duan, Tong Sun, Xinyan Fang, Zhiyong Guan, Jiafu Jiang, Sumei Chen, Weimin Fang, Fadi Chen, Shuang Zhao. Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum[J]. >Journal of Integrative Agriculture, 2025, 24(1): 176-195.
No Suggested Reading articles found!