AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (3.5 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper | Open Access

GOLDEN 2-LIKE transcription factors regulate chlorophyll biosynthesis and flavonoid accumulation in response to UV-B in tea plants

Xuyang LiuXin ChengJingjie CaoWenfeng ZhuXiaochun Wan( )Linlin Liu,( )
State Key Laboratory of Tea Plant Biology and Utilization, Key Laboratory of Tea Biology and Tea Processing of Ministry of Agriculture, Anhui Provincial Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui 230036, China

Peer review under responsibility of Chinese Society of Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS)

Show Author Information

Abstract

Flavonoids are critical secondary metabolites that determine the health benefits and flavor of tea, while chlorophylls are important contributors to the appearance of tea. However, transcription factors (TFs) that can integrate both chlorophyll biosynthesis and flavonoid accumulation in response to specific light signals are rarely identified. In this study, we report that the GOLDEN 2-LIKE TF pair, CsGLK1 and CsGLK2, orchestrate UV-B-induced responses in the chlorophyll biosynthesis and flavonoid accumulation of tea leaves. The absence of solar UV-B reduced the transcriptional expression of CsGLKs in the tea leaves and was highly correlated with a decrease in flavonoid levels (especially flavonol glycosides) and the expression of genes and TFs involved in chlorophyll biosynthesis and flavonoid accumulation. In vivo and in vitro molecular analyses showed that CsGLKs could be regulated by the UV-B signal mediator CsHY5, and could directly bind to the promoters of gene and TF involved in light-harvesting (CsLhcb), chlorophyll biosynthesis (CsCHLH, CsHEMA1, and CsPORA), and flavonoid accumulation (CsMYB12, CsFLSa, CsDFRa, and CsLARa), eventually leading to UV-B-induced responses in the chlorophylls and flavonoids of tea leaves. Furthermore, UV-B exposure increased the levels of total flavonoids, CsGLK1 protein, and expression of CsGLKs and target genes in the tea leaves. These results indicate that CsGLKs may modulate tea leaf characteristics by regulating chlorophyll biosynthesis and flavonoid accumulation in response to solar UV-B. As the first report on UV-B-induced changes in flavonoid and chlorophyll regulation mediated by CsGLKs, this study improves our understanding of the environmental regulations regarding tea quality and sheds new light on UV-B-induced flavonoid responses in higher plants.

References

 

An, X.H., Tian, Y., Chen, Y.H., Li, E.M., Li, M., Cheng, C.G., 2018. Functional identification of apple MdGLK1 which regulates chlorophyll biosynthesis in Arabidopsis. J Plant Growth, 38: 778–787.

 

Brand A., Borovsky Y., Hill T., Rahman K.A.A., Bellalou A., Van Deynze A., Paran I., 2014. CaGLK2 regulates natural variation of chlorophyll content and fruit color in pepper fruit. Theor Appl Genet, 127: 2139–2148.

 

Brown B.A., Cloix C., Jiang G.H., Kaiserli E., Herzyk P., Kliebenstein D.J., Jenkins G.I., 2005. A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA, 102: 18225–18230.

 

Chen M., Ji M., Wen B., Liu L., Li S., Chen X., Gao D., Li L., 2016. GOLDEN 2-LIKE transcription factors of plants. Front Plant Sci, 7: e1509.

 

Chen X.J., Wang P.J., Gu M.Y., Hou B.H., Zhang C.R., Zheng Y.C., Sun Y., Jin S., and Ye N.X., 2022. Identification of PAL genes related to anthocyanin synthesis in tea plants and its correlation with anthocyanin content. Hortic Plant J, 8: 381–394.

 

Dong F., Shi Y., Liu M., Fan K., Zhang Q., Ruan J., 2018. iTRAQ-based quantitative proteomics analysis reveals the mechanism underlying the weakening of carbon metabolism in chlorotic tea leaves. Int J Mol Sci, 19: e3943.

 

Fitter D.W., Martin D.J., Copley M.J., Scotland R.W., Langdale J.A., 2002. GLK gene pairs regulate chloroplast development in diverse plant species. Plant J, 31: 713–727.

 

Gangappa S.N., Botto J.F., 2016. The multifaceted roles of HY5 in plant growth and development. Mol Plant, 9: 1353–1365.

 

Hao X., Zhang W., Liu Y., Zhang H., Ren H., Chen Y., Wang L., Zeng J., Yang Y., Wang X., 2020. Pale green mutant analyses reveal the importance of CsGLKs in chloroplast developmental regulation and their effects on flavonoid biosynthesis in tea plant. Plant Physiol Biochem, 146: 392–402.

 

Hellens R.P., Allan A.C., Friel E.N., Bolitho K., Grafton K., Templeton M.D., Karunairetnam S., Gleave A.P., Laing W.A., 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1: e13.

 

Ji H.G., Lee Y.R., Lee M.S., Hwang K.H., Park C.Y., Kim E.H., Park J.S., Hong Y.S., 2018. Diverse metabolite variations in tea (Camellia sinensis L.) leaves grown under various shade conditions revisited: a metabolomics study. J Agric Food Chem, 66: 1889–1897.

 

Jiang X., Liu Y., Li W., Zhao L., Meng F., Wang Y., Tan H., Yang H., Wei C., Wan X., Gao L., Xia T., 2013. Tissue-specific, development-dependent phenolic compounds accumulation profile and gene expression pattern in tea plant [Camellia sinensis]. PLoS One, 8: e62315.

 

Kan Z., Wang Y., Chen Q., Tang X., Thompson H.J., Huang J., Zhang J., Gao F., Shen Y., Wan X., 2021. Green tea suppresses amyloid β levels and alleviates cognitive impairment by inhibiting APP cleavage and preventing neurotoxicity in 5XFAD mice. Mol Nutr Food Res, 65: e2100626.

 

Kobayashi K., Baba S., Obayashi T., Sato M., Toyooka K., Keränen M., Aro E.-M., Fukaki H., Ohta H., Sugimoto K., Masuda T., 2012. Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell, 24: 1081–1095.

 

Kobayashi K., Obayashi T., Masuda T., 2014. Role of the G-box element in regulation of chlorophyll biosynthesis in Arabidopsis roots. Plant Signal Behav, 7: 922–926.

 

Lee L.S., Choi J.H., Son N., Kim S.H., Park J.D., Jang D.J., Jeong Y., Kim H.J., 2013. Metabolomic analysis of the effect of shade treatment on the nutritional and sensory qualities of green tea. J Agric Food Chem, 61: 332–338.

 

Li H., Li Y., Deng H., Sun X., Wang A., Tang X., Gao Y., Zhang N., Wang L., Yang S., Liu Y., Wang S., 2018. Tomato UV-B receptor SlUVR8 mediates plant acclimation to UV-B radiation and enhances fruit chloroplast development via regulating SlGLK2. Sci Rep, 8: 6097–6109.

 

Liang T., Mei S., Shi C., Yang Y., Peng Y., Ma L., Wang F., Li X., Huang X., Yin Y., Liu H., 2018. UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Dev Cell, 44: 512–523.

 

Lin N., Liu X., Zhu W., Cheng X., Wang X., Wan X., Liu L., 2021. Ambient ultraviolet B signal modulates tea flavor characteristics via shifting a metabolic flux in flavonoid biosynthesis. J Agric Food Chem, 69: 3401–3414.

 

Liu L., Gregan S., Winefield C., Jordan B., 2015. From UVR8 to flavonol synthase: UV-B-induced gene expression in Sauvignon blanc grape berry. Plant Cell Environ, 38: 905–919.

 

Liu L., Li Y., She G., Zhang X., Jordan B., Chen Q., Zhao J., Wan X., 2018a. Metabolite profiling and transcriptomic analyses reveal an essential role of UVR8-mediated signal transduction pathway in regulating flavonoid biosynthesis in tea plants (Camellia sinensis) in response to shading. BMC Plant Biol, 18: e233.

 

Liu L., Lin N., Liu X., Yang S., Wang W., Wan X., 2020. From chloroplast biogenesis to chlorophyll accumulation: the interplay of light and hormones on gene expression in Camellia sinensis cv. Shuchazao leaves. Front Plant Sci, 11: e00256.

 

Liu X., Li L., Li M., Su L., Lian S., Zhang B., Li X., Ge K., Li L., 2018b. AhGLK1 affects chlorophyll biosynthesis and photosynthesis in peanut leaves during recovery from drought. Sci Rep, 8: e2250.

 

Liu X., Li Y., Zhong S., 2017. Interplay between light and plant hormones in the control of Arabidopsis seedling chlorophyll biosynthesis. Front Plant Sci, 8: e01433.

 

Loyola R., Herrera D., Mas A., Wong D.C.J., Höll J., Cavallini E., Amato A., Azuma A., Ziegler T., Aquea F., Castellarin S.D., Bogs J., Tornielli G.B., Peña-Neira A., Czemmel S., Alcalde J.A., Matus J.T., Arce-Johnson P., 2016. The photomorphogenic factors UV-B RECEPTOR 1, ELONGATED HYPOCOTYL 5, and HY5 HOMOLOGUE are part of the UV-B signalling pathway in grapevine and mediate flavonol accumulation in response to the environment. J Exp Bot, 67: 5429–5445.

 

Nan H., Lin Y.L., Wang X.H, and Gao L.Z., 2021. Comprehensive genomic analysis and expression profiling of cysteine-rich polycomb-like transcription factor gene family in tea Tree. Hortic Plant J, 7: 469–478.

 

Ng K.-W., Cao Z.-J., Chen H.-B., Zhao Z.-Z., Zhu L., Yi T., 2017. Oolong tea: a critical review of processing methods, chemical composition, health effects, and risk. Crit Rev Food Sci Nutr, 58: 2957–2980.

 

Reinbothe S., Reinbothe C., Lebede N., Apela K., 1996. PORA and PORB, two light-dependent protochlorophyllide-reducing enzymes. Plant Cell, 8: 763–769.

 

Stracke R., Favory J.-J., Gruber H., Bartelniewoehner L., Bartels S., Binkert M., Funk M., Weisshaar B., Ulm R., 2010. The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ, 33: 88–103.

 

Tanaka R., Kobayashi K., Masuda T., 2011. Tetrapyrrole metabolism in Arabidopsis thaliana. The Arabidopsis Book, 9: e0145.

 

Tanaka R., Tanaka A., 2007. Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol, 58: 321–346.

 

Tang X., Miao M., Niu X., Zhang D., Cao X., Jin X., Zhu Y., Fan Y., Wang H., Liu Y., Sui Y., Wang W., Wang A., Xiao F., Giovannoni J., Liu Y., 2015. Ubiquitin-conjugated degradation of golden 2-like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato. New Phytol, 209: 1028–1039.

 

Tilbrook K., Arongaus A.B., Binkert M., Heijde M., Yin R., Ulm R., 2013. The UVR8 UV-B photoreceptor: perception, signaling and response. The Arabidopsis Book, 11: e0164.

 

Wang N., Xu H., Jiang S., Zhang Z., Lu N., Qiu H., Qu C., Wang Y., Wu S., Chen X., 2017. MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant J, 90: 276–292.

 

Wang P., Fouracre J., Kelly S., Karki S., Gowik U., Aubry S., Shaw M.K., Westhoff P., Slamet-Loedin I.H., Quick W.P., Hibberd J.M., Langdale J.A., 2012a. Evolution of GOLDEN2-LIKE gene function in C3 and C4 plants. Planta, 237: 481–495.

 

Wang W., Zhou Y., Wu Y., Dai X., Liu Y., Qian Y., Li M., Jiang X., Wang Y., Gao L., Xia T., 2018. Insight into catechins metabolic pathways of Camellia sinensis based on genome and transcriptome analysis. J Agric Food Chem, 66: 4281–4293.

 

Wang Y., Gao L., Shan Y., Liu Y., Tian Y., Xia T., 2012b. Influence of shade on flavonoid biosynthesis in tea (Camellia sinensis (L.) O. Kuntze). Sci Hortic, 141: 7–16.

 

Waters M.T., Moylan E.C., Langdale J.A., 2008. GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J, 56: 432–444.

 

Waters M.T., Wang P., Korkaric M., Capper R.G., Saunders N.J., Langdale J.A., 2009. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell, 21: 1109–1128.

 

Wei C., Yang H., Wang S., Zhao J., Liu C., Gao L., Xia E., Lu Y., Tai Y., She G., Sun J., Cao H., Tong W., Gao Q., Li Y., Deng W., Jiang X., Wang W., Chen Q., Zhang S., Li H., Wu J., Wang P., Li P., Shi C., Zheng F., Jian J., Huang B., Shan D., Shi M., Fang C., Yue Y., Li F., Li D., Wei S., Han B., Jiang C., Yin Y., Xia T., Zhang Z., Bennetzen J.L., Zhao S., Wan X., 2018. Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proc Natl Acad Sci USA, 115: 4151–4158.

 

Xia, E.H., Tong, W., Wu, Q., Wei, S., Zhao, J., Zhang, Z.Z., Wei, C.L., Wan, X.C., 2020. Tea plant genomics: achievements, challenges and perspectives. Hortic Res, 7: 7.

 

Xia E.H., Li F.D., Tong W., Li P.H., Wu Q., Zhao H.J., Ge R.H., Li R.P., Li Y.Y., Zhang Z.Z., Wei C.L., Wan X.C., 2019. Tea plant information archive: a comprehensive genomics and bioinformatics platform for tea plant. Plant Biotechnol J, 17: 1938–1953.

 

Xu N., Chu J., Dong R., Lu F., Zhang X., Wang M., Shen Y., Xie Z., Ho C.T., Yang C.S., Wang Y., Wan X., 2021. Yellow tea stimulates thermogenesis in mice through heterogeneous browning of adipose tissues. Mol Nutr Food Res, 65: e2000864.

 

Xu N., Chu J., Wang M., Chen L., Zhang L., Xie Z., Zhang J., Ho C.-T., Li D., Wan X., 2018. Large yellow tea attenuates macrophage-related chronic inflammation and metabolic syndrome in high-fat diet treated mice. J Agric Food Chem, 66: 3823–3832.

 

Xu W., Dubos C., Lepiniec L., 2015. Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends Plant Sci, 20: 176–185.

 

Yang T., Li H., Tai Y., Dong C., Cheng X., Xia E., Chen Z., Li F., Wan X., Zhang Z., 2020. Transcriptional regulation of amino acid metabolism in response to nitrogen deficiency and nitrogen forms in tea plant root (Camellia sinensis L.). Sci Rep, 10: 6868.

 

Zhang C., Wang M., Gao X., Zhou F., Shen C., Liu Z., 2020a. Multi-omics research in albino tea plants: past, present, and future. Sci Hortic, 261: e108943.

 

Zhang L., Cao Q.Q., Granato D., Xu Y.Q., Ho C.T., 2020b. Association between chemistry and taste of tea: a review. Trends Food Sci Technol, 101: 139–149.

 

Zhang Q., Liu M., Ruan J., 2017a. Integrated transcriptome and metabolic analyses reveals novel insights into free amino acid metabolism in Huangjinya tea cultivar. Front Plant Sci, 8: e291.

 

Zhang X., Huai J., Shang F., Xu G., Tang W., Jing Y., Lin R., 2017b. A PIF1/PIF3-HY5-BBX23 transcription factor cascade affects photomorphogenesis. Plant Physiol, 174: 2487–2500.

 

Zhang X., Wu H., Chen L., Liu L., Wan X., 2018. Maintenance of mesophyll potassium and regulation of plasma membrane H+-ATPase are associated with physiological responses of tea plants to drought and subsequent rehydration. Crop J, 6: 611–620.

 

Zhao, X., Zeng, X., Lin, N., Yu, S., Fernie, A.R., Zhao, J., 2021. CsbZIP1-CsMYB12 mediates the production of bitter-tasting flavonols in tea plants (Camellia sinensis) through a coordinated activatorerepressor network. Hortic Res, 8: 110.

Horticultural Plant Journal
Pages 1055-1066
Cite this article:
Liu X, Cheng X, Cao J, et al. GOLDEN 2-LIKE transcription factors regulate chlorophyll biosynthesis and flavonoid accumulation in response to UV-B in tea plants. Horticultural Plant Journal, 2023, 9(5): 1055-1066. https://doi.org/10.1016/j.hpj.2023.04.002

253

Views

6

Downloads

2

Crossref

2

Web of Science

2

Scopus

0

CSCD

Altmetrics

Received: 20 October 2022
Revised: 25 November 2022
Accepted: 13 March 2023
Published: 05 April 2023
© 2023 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return