A G6P1E isomerase of sugar metabolism is involved in the flower colors of Dianthus chinensis
Heng Zhang
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR Chinahttps://orcid.org/0000-0003-0774-2210
Ya-Nan Gao
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR Chinahttps://orcid.org/0000-0002-7973-2241
Xue-Qin He
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR Chinahttps://orcid.org/0000-0002-3700-5273
Abstract
Dianthus chinensis L. is indigenous to northern China, Korea, Mongolia, Kazakhstan, and southeastern Russia. It is widely cultivated in urban landscapes. Its flower has a great variety of colors and color schemes. Sugars control and induce anthocyanin synthesis and accumulation in plants. In sugar metabolism, many enzymes are specific for their substrate’s α or β anomer. Gaining and characterizing genes involved in sugar metabolism and flower color will be beneficial in clarifying the role of sugar in the flower colors of D. chinensis. Glucose-6-phosphate-1-epimerase (G6P1E, EC 5.1.3.15) catalyzes the α or β change of glucose-6-phosphate at the branch point of glucose metabolism. DchG6P1E1 (MZ292712) was isolated in D. chinensis and characterized using the tobacco rattle virus (TRV)-based virus-induced gene silencing (VIGS) system. Its cDNA full length is 1401 bp, including an open reading frame of 918 bp. In the DchG6P1E1-silenced flowers, the reducing purple was observed, as well as the anthocyanin content, reducing sugar content, G6P1E activity, and DchG6P1E1 expression were significantly decreased. During the development of floral buds and among the three flower colors, the anthocyanin content, reduced sugar content, G6P1E activity, and DchG6P1E1 expression rose dramatically, with pigments increasing in the petals. Among the organs, the flowers had the highest anthocyanin contents and reducing sugar. The highest levels of G6P1E activity and DchG6P1E1 expression were in the roots. The anthocyanin content was positively related to the reducing sugar content at 0.05 levels by correlation analysis. In conclusion, DchG6P1E1 is a root-enriched gene associated with flower colors in D. chinensis.
Keywords:
Dianthus chinensis , virus-induced gene silencing, G6P1E, anthocyanin content, reducing sugar contentReferences
Baek, S., Choi, K., Kim, G.B., Yu, H.J., Cho, A., Jang, H., Kim, C., Kim, H.J., Chang, K.S., Kim, J.H., Mun, J.H. (2018). Draft genome sequence of wild Prunus yedoensis reveals massive inter-specific hybridization between sympatric flowering cherries. Genome Biol., 19, 1–17. https://doi.org/10.1186/s13059-018-1497-y DOI: https://doi.org/10.1186/s13059-018-1497-y
Bridge, A., Axelsen, K. (2024). Enzyme nomenclature database, https://enzyme.expasy.org/ enzyme-byclass. html [date of access: 8.02.2024].
Deng, X., Bashandy, H., Ainasoja, M., Kontturi, J., Pietiäinen, M., Laitinen, R.A.E., Albert, V.A., Valkonen, J.P.T., Elomaa, P., Teeri, T.H. (2014). Functional diversification of duplicated chalcone synthase genes in anthocyanin biosynthesis of Gerbera hybrida. New Phytol., 201(4), 1469–1483. https://doi.org/10.1111/nph.12610 DOI: https://doi.org/10.1111/nph.12610
Donoso, A., Rivas, C., Zamorano, A., Peña, Á., Handford, M., Aros, D. (2021). Understanding Alstroemeria pallida flower colour: links between phenotype, anthocyanins and gene expression. Plants, 10(1), 55. https://doi.org/10.3390/plants10010055 x DOI: https://doi.org/10.3390/plants10010055
Feng, H., Fan, X., Miller, A.J., Xu, G. (2020). Plant nitrogen uptake and assimilation: regulation of cellular pH homeostasis. J. Exp. Bot., 71(15), 4380–4392. https://doi.org/10.1093/jxb/eraa150 DOI: https://doi.org/10.1093/jxb/eraa150
Fu, X.P., Ning, G.G., Gao, L.P., Bao, M.Z. (2008). Genetic diversity of Dianthus accessions as assessed using two molecular marker systems (SRAPs and ISSRs) and morphological traits. Sci. Hort., 117(3), 263–270. https://doi.org/10.1016/j.scienta.2008.04.001 DOI: https://doi.org/10.1016/j.scienta.2008.04.001
Graille, M., Baltaze, J.P., Leulliot, N., Liger, D., Quevillon-Cheruel, S., van Tilbeurgh, H. (2006). Structurebased functional annotation: Yeast ymr099c codes for a D-hexose-6-phosphate mutarotase. J. Biol. Chem., 281(40), 30175–30185. https://doi.org/10.1074/jbc.M604443200 DOI: https://doi.org/10.1074/jbc.M604443200
Hiratsuka, S., Onodera, H., Kawai, Y., Kubo, T., Itoh, H., Wada, R. (2001). ABA and sugar effects on anthocyanin formation in grape berry cultured in vitro. Sci. Hortic., 90, 121–130. https://doi.org/10.1016/ S0304-4238(00)00264-8 DOI: https://doi.org/10.1016/S0304-4238(00)00264-8
Hu, D.G., Sun, C.H., Zhang, Q.Y., An, J.P., You, C.X., Hao, Y.J. (2016). Glucose sensor MdHXK1 phosphorylates and stabilizes MdbHLH3 to promote anthocyanin biosynthesis in apple. PLoS Genet., 25, e1006273. https://doi.org/10.1371/journal.pgen.1006273 DOI: https://doi.org/10.1371/journal.pgen.1006273
Jin, L., Yang, G., Tan, C., Zhao, C. (2015). Effects of nitrogen stress on the photosynthetic CO2 assimilation, chlorophyll fluorescence and sugar-nitrogen ratio in corn. Sci. Rep., 5, 9311. https://doi.org/0.1038/srep09311 DOI: https://doi.org/10.1038/srep09311
Kantia, A., Kothari, S. (2002). High efficiency adventitious shoot bud formation and plant regeneration from leaf explants of Dianthus chinensis L. Sci. Hortic., 96, 205–212. https://doi.org/10.1016/S0304- 4238(02)00081-X DOI: https://doi.org/10.1016/S0304-4238(02)00081-X
Lejay, L., Wirth, J., Pervent, M., Cross, J.M.F., Tillard, P., Gojon, A. (2008). Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol., 146(4), 2036–2053. https://doi.org/10.1104/pp.107.114710 DOI: https://doi.org/10.1104/pp.107.114710
Lim, T.K. (2014). Edible medicinal and non-medicinal plants. Vol. 7, Flowers. Springer, Heidelberg, 694–697. https://doi.org/10.1007/978-94-007-7395-0 DOI: https://doi.org/10.1007/978-94-007-7395-0_49
Liu, J., Hao, X.L., He, X.Q. (2021). Characterization of three chalcone synthase-like genes in Dianthus chinensis. Plant Cell Tiss. Org. Cult., 146(1), 483–492. https://doi.org/10.1007/s11240-021-02081-8 DOI: https://doi.org/10.1007/s11240-021-02081-8
Livak, K.J., Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2C-ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262 DOI: https://doi.org/10.1006/meth.2001.1262
Luo, B., Ma, P., Nie, Z., Zhang X., He X., Ding X., Feng X., Lu Q., Ren Z., Lin H., Wu Y., Shen Y, Zhang S., Wu L., Liu D., Pan G., Rong T., Gao S. (2019a). Metabolite profiling and genome-wide association studies reveal response mechanisms of phosphorus deficiency in
maize seedling. Plant J., 97(5), 947–969. https://doi.org/10.1111/tpj.14160 DOI: https://doi.org/10.1111/tpj.14160
Luo, Y., Lin, Y., Mo, F., Ge, C., Jiang, L., Zhang, Y., Chen, Q., Sun, B., Wang, Y., Wang, X., Tang, H. (2019b). Sucrose promotes strawberry fruit ripening and affects ripening-related processes. Int. J. Genomics, 2019, 1–14. https://doi.org/10.1155/2019/9203057 DOI: https://doi.org/10.1155/2019/9203057
Nakatsuka, A., Izumi, Y., Yamagishi, M. (2003). Spatial and temporal expression of chalcone synthase and dihydroflavonol 4-reductase genes in the Asiatic hybrid lily. Plant Sci., 165(4), 759–767. https://doi.org/10.1016/S0168-9452(03)00254-1 DOI: https://doi.org/10.1016/S0168-9452(03)00254-1
Ohno, S., Hosokawa, M., Kojima, M., Kitamura, Y., Hoshino, A., Tatsuzawa, F., Doi, M., Yazawa, S. (2011). Simultaneous post-transcriptional gene silencing of two different chalcone synthase genes resulting in pure white flowers in the octoploid dahlia. Planta, 234, 945–958. https://doi.org/10.1007/s00425-011-1456-2 DOI: https://doi.org/10.1007/s00425-011-1456-2
Ou, C.Q., Wang, F., Wang, J.H., Li, S., Zhang, Y.J., Fang, M., Ma, L., Zhao, Y.N., Jiang, S.L. (2019). A de novo genome assembly of the dwarfing pear rootstock Zhongai 1. Sci. Data, 6, 281. https://doi.org/10.1038/s41597-019-0291-3 DOI: https://doi.org/10.1038/s41597-019-0291-3
Rabino, I., Mancinelli, A.L. (1986). Light, temperature, and anthocyanin production. Plant physiol., 81, 922–924. https://doi.org/10.1104/pp.81.3.922 DOI: https://doi.org/10.1104/pp.81.3.922
Rascher, U., Liebig, M., Lüttge, U. (2000). Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant Cell Environ., 23, 1397–1405. https://doi.org/10.1046/j.1365-3040.2000.00650.x DOI: https://doi.org/10.1046/j.1365-3040.2000.00650.x
Raven, J.A. (2022). Interactions between above and below ground plant structures: mechanisms and ecosystem services. Front. Agr. Sci. Eng., 9, 197–213. https://doi.org/10.15302/J-FASE-2021433 DOI: https://doi.org/10.15302/J-FASE-2021433
Shang, Y.J., Schwinn, K.E., Bennett, M.J., Hunter, D.A., Waugh, T.L., Pathirana, N.N., Brummell, D.A., Jameson, P.E., Davies, K.M. (2007). Methods for transient assay of gene function in floral tissues. Plant Methods, 3, 1–12. https://doi.org/10.1186/1746-4811-3-1 DOI: https://doi.org/10.1186/1746-4811-3-1
Shimizu, T., Tanizawa, Y., Mochizuki, T., Nagasaki, H., Yoshioka, T., Toyoda, A., Fujiyama, A., Kaminuma, E., Nakamura, Y. (2017). Draft sequencing of the heterozygous diploid genome of satsuma (Citrus unshiu Marc.) using a hybrid assembly approach. Front. Genet., 8, 180. https://doi.org/10.3389/fgene. 2017.00180 DOI: https://doi.org/10.3389/fgene.2017.00180
Sierkstra, L.N., Sillje, H.H.W., Verbakel, J.M.A., Verrips, C.T. (1993). The glucose-6-phosphate-isomerase reaction is essential for normal glucose repression in Saccharomyces cerevisiae. Eur. J. Biochem., 214, 121–127. https://doi.org/10.1111/j.1432-1033.1993.tb17903.x DOI: https://doi.org/10.1111/j.1432-1033.1993.tb17903.x
Sui, X., Zhao, M., Xu, Z., Zhao, L., Han, X. (2018). RrGT2, a key gene associated with anthocyanin biosynthesis in Rosa rugosa, was identified via virus-induced gene silencing and overexpression. Int. J. Mol. Sci., 19, 4057. https://doi.org/10.3390/ijms19124057 DOI: https://doi.org/10.3390/ijms19124057
Sun, M., Feng, X.X., Gao, J.J., Peng, R.H., Yao, Q.H., Wang, L.J. (2017). VvMYBA6 in the promotion of anthocyanin biosynthesis and salt tolerance in transgenic Arabidopsis. Plant Biotechnol. Rep., 11, 299–314. https://doi.org/10.1007/s11816-017-0452-9 DOI: https://doi.org/10.1007/s11816-017-0452-9
Suzuki, K., Suzuki, T., Nakatsuka, T., Dohra, H., Yamagishi, M., Matsuyama, K., Matsuura, H. (2016). RNA-seqbased evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies (Lilium spp.). BMC Genomics, 17, 611–629. https://doi.org/10.1186/s12864-016-2995-5 DOI: https://doi.org/10.1186/s12864-016-2995-5
Wood, T.M., Bhat, K.M. (1988). Methods for measuring cellulase activities. Method Enzymol., 160, 87–112. https://doi.org/10.1016/0076-6879(88)60109-1 DOI: https://doi.org/10.1016/0076-6879(88)60109-1
Zhang, L.Y., Hu, J., Han, X.L., Li, J.J., Gao, Y., Richards, C.M., Zhang, C.X., Tian, Y., Liu, G.M., Gul, H., Wang, D.J., Tian, Y., Yang, C.X., Meng, M.H., Yuan, G.P., Kang, G.D., Wu, Y.L., Wang, K., Zhang, H,T., Wang, D.P., Cong, P.H. (2019). A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat. Commun., 10, 1494. https://doi.org/10.1038/s41467-019-09518-x DOI: https://doi.org/10.1038/s41467-019-09518-x
Zhou, Y., Gao, Y.G., Giusti, M.M. (2020). Accumulation of anthocyanins and other phytochemicals in American elderberry cultivars during fruit ripening and its impact on color expression. Plants, 9, 1721. https://doi.org/10.3390/plants9121721 DOI: https://doi.org/10.3390/plants9121721
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR China https://orcid.org/0000-0003-0774-2210
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR China https://orcid.org/0000-0002-7973-2241
College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010019, PR China https://orcid.org/0000-0002-3700-5273
License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.
