Abstract
The fruit skin color is an important economic trait of blueberries (Vaccinium spp.) and is determined by the concentration of anthocyanins. Light intensity significantly affects anthocyanin accumulation. Anthocyanin content is closely related to enzyme activity and gene expression. In this study, the anthocyanin content, the activity of related enzymes and the expression of genes involved in the development process of 5-year ‘Pink Blue’ cranberry were studied. The results showed that with increasing light intensity, the content of anthocyanin glycosides increased, while that of flavonoids, chlorophylls and carotenoids decreased. Except for chalcone isomerases (CHI) and flavonol synthetases (FLS), all enzymes involved in anthocyanin synthesis showed the same trend as anthocyanin glycosides. The expression of genes for transcription factors, such as VcMYB1 and VcbHLH004, and certain photoreceptor factors were significantly downregulated under shading conditions. Correlation analysis showed that flavonoid 3',5'-hydroxylase (F3'5'H) and VcF3'5'H4 are the key enzymes for anthocyanin glycoside synthesis in blueberry as well as the corresponding enzyme genes. This study provides a foundation for further research on the mechanism of light-induced anthocyanin synthesis in blueberry.
Similar content being viewed by others
REFERENCES
Zhao, Y., Dong, W., Wang, K., Zhang, B., Allan, A.C., Lin-Wang, K., Chen, K., and Xu, C., Differential sensitivity of fruit pigmentation to ultraviolet light between two peach cultivars, Front. Plant Sci., 2017, vol. 8, p. 1552. https://doi.org/10.3389/fpls.2017.01552
He, Y.J., Chen. H., Zhou. L., Liu, Y., and Chen, H.Y., Comparative transcription analysis of photosensitive and non-photosensitive eggplants to identify genes involved in dark regulated anthocyanin synthesis, BMC Genomics, 2019, vol. 20, p. 678. https://doi.org/10.1186/s12864-019-6023-4
Albert, N.W., Lewis. D.H., Zhang, H., Irving, L.J., Jameson, P.E., and Davies, K.M., Light-induced vegetative anthocyanin pigmentation in Petunia, J. Exp. Bot., 2009, vol. 60, p. 2191. https://doi.org/10.1093/jxb/erp097
Jaakola, L., New insights into the regulation of anthocyanin biosynthesis in fruits, Trends Plant Sci., 2013, vol. 18, p. 477. https://doi.org/10.1016/j.tplants.2013.06.003
Zoratti, L., Karppinen, K., Luengo Escobar A., Häggman, H., and Jaakola, L., Light-controlled flavonoid biosynthesis in fruits, Front. Plant Sci., 2014, vol. 5, p. 534. https://doi.org/10.3389/fpls.2014.00534
Macheix, J.J., Fleuriet, A., and Billot, J., Fruit Phenolics, Boca Raton: CRC Press, Florida, USA, 1990, p. 378.
Xu, P.B., Zawora, C., Li, Y., Wu, J., Liu, L.C., Liu, Z.C., Cai, R., and Lian, H.L., Transcriptome sequencing reveals role of light in promoting anthocyanin accumulation of strawberry fruit, Plant Growth Regul., 2018, vol. 86, p. 121. https://doi.org/10.1007/s10725-018-0415-3
Li, T., Yamane, H., and Tao, R., Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifes stage-specifc anthocyanin metabolism in highbush blueberry, Hortic. Res., 2021, vol. 8, p. 67. https://doi.org/10.1038/s41438-021-00503-4
Nguyen, H.M., Putterill, J., Dare, A.P., Plunkett, B.J., Cooney, J., Peng, Y.Y., Souleyre, E.J.F., Albert, N.W., Espley, R.V., and Günther, C.S., Two genes, ANS and UFGT2, from Vaccinium spp. are key steps for modulating anthocyanin production, Front. Plant Sci., 2023, vol. 14, p. 1082246. https://doi.org/10.3389/fpls.2023.1082246
Bennett, C., Sookwong, P., Jakmunee, J., and Mahatheeranont, S., Smartphone digital image colorimetric determination of the total monomeric anthocyanin content in black rice via the pH differential method, Anal. Methods, 2021, vol. 13, p. 3348. https://doi.org/10.1039/d1ay00719j
Tian, T., Qiao, G., Deng, B., Wen, Z., Hong, Y., and Wen, X.P., The effects of rain shelter coverings on the vegetative growth and fruit characteristics of Chinese cherry (Prunus pseudocerasus Lindl.), Sci. Hortic. (Amsterdam, Neth.), 2019, vol. 254, p. 228. https://doi.org/10.1016/j.scienta.2019.04.030
Schraer, S.M., Shaw, D.R., Boyette, M., Coupe, R.H., and Thurman M.E., Comparison of enzyme-linked immunosorbent assay and gas chromatography procedures for the detection of cyanazine and metolachlor in surface water samples, J. Agric. Food Chem., 2000, vol. 48, p. 5881. https://doi.org/10.1021/jf991130y
Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method, Methods, 2001, vol. 25, p. 402. https://doi.org/10.1006/meth.2001.1262
Azuma, A., Yakushiji, H., Koshita, Y., and Kobayashi, S., Flavonoid biosynthesis-related genes in grape skin are dirfferentially regulated by temperature and light conditions, Planta, 2012, vol. 236, p. 1067. https://doi.org/10.1007/s00425-012-1650-x
Sun, L., Li, S.C., Tang, X.P., Fan, X.C., Zhang, Y., Jiang, J.F., Liu, J., and Liu, C.H., Transcriptome analysis reveal the putative genes involved in light-induced anthocyanin accumulation in grape ‘Red Globe’ (V. vinifera L.), Gene, 2020, vol. 728, p. 144284. https://doi.org/10.1016/j.gene.2019.144284
Li, Y.Y., Mao, K., Zhao, C., Zhao, X.Y., Zhang, H.L., Shu, H.R., and Hao, Y.J., MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple, Plant Physiol., 2012, vol. 160, p. 1011. https://doi.org/10.1104/pp.112.199703
Zhang, H.N., Li, W.C., Wang, H.C., Shi, S.Y., Shu, B., Liu, L.Q., Wei, Y.Z., and Xie, J.H., Transcriptome profiling of light-regulated anthocyanin biosynthesis in the pericarp of litchi, Front. Plant Sci., 2016, vol. 7, p. 963. https://doi.org/10.3389/fpls.2016.00963
Yamagishi, M., A novel R2R3-MYB transcription factor regulates light-mediated floral and vegetative anthocyanin pigmentation patterns in Lilium regale, Mol. Breed., 2016, vol. 36, p. 3. https://doi.org/10.1007/s11032-015-0426-y
Lipphardt, S., Brettschneider, R., Kreuzaler, F., Schell, J., and Dangl, J.L., UV-inducible transient expression in parsley protoplasts identifies regulatory cis-elements of a chimeric Antirrhinum majus chalcone synthase gene, EMBO J., 1988, vol. 7, p. 4027. https://doi.org/10.1002/j.1460-2075.1988.tb03296.x
Wang, Y.S., Xu, Y.J., Gao, L.P., Yu, O., Wang, X.Z., He, X.J., Jiang, X.L., Liu, Y.J., and Xia, T., Functional analysis of flavonoid 3’,5’-hydroxylase from tea plant (Camellia sinensis): critical role in the accumulation of catechins, BMC Plant Biol., 2014, vol. 14, p. 347. https://doi.org/10.1186/s12870-014-0347-7
Fu, Z.Z., Shang, H.Q., Jiang, H., Gao, J., Dong, X.Y., Wang, H.J., Yi, Y.M., Wang, L.M., Zhang, J., Shu, Q.Y., Chao Y.C., Xu, M.L., Wang, R., Wang, L.S., and Zhang, H.C., Systematic identification of the light-quality responding anthocyanin synthesis-related transcripts in petunia petals, Hortic. Plant J., 2020, vol. 6, p. 428. https://doi.org/10.1016/j.hpj.2020.11.006
Ma, Z., Li, W., Mao, J., Li, W., Zuo, C.W., Zhao, X., Dawuda, M.M., Shi, X.Y., and Chen, B.H., Synthesis of light-inducible and light-independent anthocyanins regulated by specific genes in grape ‘Marselan’ (V. vinifera L.), Peer J., 2019, vol. 7, p. 6521. https://doi.org/10.7717/peerj.6521
Daniela, R., Espley, R.V., Henry-Kirk, R.A., Andreotti, C., Ziosi, V., Hellens, R.P., Costa, G., and Allan, A.C., Transcriptional regulation of flavonoid biosynthesis in nectarine (prunus persica) by a set of R2R3 MYB transcription factors, BMC Plant Biol., 2013, vol. 13, p. 68. https://doi.org/10.1186/1471-2229-13-68
Bai, S.L., Tao, R.Y., Tang, Y.X., Yin, L., Ma, Y.J., Ni, J.B., Yan, X.H., Yang, Q.S., Wu, Z.Y., Zeng, Y.L., and Teng, Y.W., BBX16, a B-box protein, positively regulates light-induced anthocyanin accumulation by activating MYB10 in red pear, Plant Biotechnol. J., 2019, vol. 17, p. 1985. https://doi.org/10.1111/pbi.13114
Li, L.Z., Li, S.H., Ge, H.Y., Shi, S.L., Li, D.L., Liu, Y., and Chen, H.Y., A light-responsive transcription factor SmMYB35 enhances anthocyanin biosynthesis in eggplant (Solanum melongena L.), Planta, 2022, vol. 255, p. 12. https://doi.org/10.1007/s00425-021-03698-x
Xu, W., Dubos, C., and Lepiniec, L., Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes, Trends in Plant Sci., 2015, vol. 20, p. 176. https://doi.org/10.1016/j.tplants.2014.12.001
Cominelli, E., Gusmaroli, G., Allegra, D., Galbiati, M., Wade, H.K., Jenkins, G.I., and Tonelli, C., Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana, J. Plant Physiol., 2018, vol. 165, p. 886. https://doi.org/10.1016/j.jplph.2007.06.010
Tao, R.Y., Yu, W.J., Gao, Y.H., Ni, J.B., Yin, L., Zhang, X., Li, H.X., Wang, D.S., Bai, S.L., and Teng, Y.W., Light-induced basic/helix-loop-helix64 enhances anthocyanin biosynthesis and undergoes CONSTITUTIVELY PHOTOMORPHOGENIC1- mediated degradation in pear, Plant Physiol., 2020, vol. 184, p. 1684. https://doi.org/10.1104/pp.20.01188
Funding
This work was supported by the National Natural Science Foundation of China (31760205) and Guangdong Basic and Applied Basic Research Foundation of Guangdong Province-Yuehui Joint Foundation (grant no. 2022A1515111095), Doctoral program of Huizhou University (2022JB021), Huizhou social science co-construction project (XJ2023000601), and the project of the Department of Education of Guangdong Province (grant no. 2018KTSCX214).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
COMPLIANCE WITH ETHICAL STANDARDS
This article does not contain any studies involving animals or human participants as objects of research.
CONFLICT OF INTEREST
The authors declare that they have no conflicts of interest.
Additional information
Abbreviations: ANOVA—analysis of variance; ANS—anthocyanin synthase; Ant—anthocyanin; CHS—chalcone synthase; CHI—chalcone isomerase; DAF—days after flowering; DFR—dihydroflavonol 4-reductase; ELISA—enzyme-linked immunosorbent assay; Fla—flavonoids; FLS—flavonol synthase; F3'H—flavonoid 3'-hydroxylase; F3'5'H—flavonoid 3',5'-hydroxylase; PAL—phenylalanine ammonia-lyase; UFGT—flavonoid 3-O-glycosyltransferase.
Supplementary Information
Rights and permissions
About this article
Cite this article
Guo, X.L., Hu, J.B. & Wang, D.L. Effect of Light Intensity on Blueberry Fruit Coloration, Anthocyanin Synthesis Pathway Enzyme Activity, and Gene Expression. Russ J Plant Physiol 70, 136 (2023). https://doi.org/10.1134/S1021443723601064
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1134/S1021443723601064