Antocyanidin-3- O -Glucosyltransferase Genes in Pepper ( Capsicum  spp.) and Their Role in Anthocyanine Biosynthesis

M. A. Filyushin; Филюшин М. А.; A. V. Shchennikova; Щенникова А. В.; E. Z. Kochieva; Кочиева Е. З.

doi:10.31857/S0016675823050041

Antocyanidin-3-O-Glucosyltransferase Genes in Pepper (Capsicum spp.) and Their Role in Anthocyanine Biosynthesis

Authors: Filyushin M.A.¹, Shchennikova A.V.¹, Kochieva E.Z.¹
Affiliations:
1. Federal Research Centre “Fundamentals of Biotechnology” of the Russian Academy of Sciences
Issue: Vol 59, No 5 (2023)
Pages: 517-529
Section: ГЕНЕТИКА РАСТЕНИЙ
URL: https://journals.rcsi.science/0016-6758/article/view/134586
DOI: https://doi.org/10.31857/S0016675823050041
EDN: https://elibrary.ru/FNOPBO
ID: 134586

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Abstract

In pepper (Capsicum spp.), anthocyanins are important not only for the photolabile compounds protection, but also for the regulation of fruit color pattern. Anthocyanidin-3-O-glucosyltransferases (UFGTs) play a key role in the biosynthesis of stable anthocyanins. In this work, the structure and phylogeny of three pepper UFGT homologue genes are characterized. Biochemical analysis of C. annuum cultivars (cv. Syrenevii cube, Othello and Sibiryak) and C. frutescens (cv. Samotsvet), which differ in the pattern of fruit pigmentation during ripening, showed the presence of anthocyanins in leaves and fruit peel of all accessions (except for the cv. Sibiryak fruit). The highest anthocyanins content was found in the purple leaves of the cv. Samotsvet. In the fruit peel of all accessions, the anthocyanins content decreased with ripening. Expression analysis of the same tissues showed that UFGT1 (LOC107843659) and UFGT2 (LOC107843660) transcripts are present in the leaves of all cultivars. In the fruit peel, UFGT1 transcripts were detected at maturation stages 1 (cv. Syrenevii cube and Othello) and 1–3 (cv. Samotsvet), while UFGT2 transcripts were found in all accessions with the maximum in the cv. Sibiryak, where anthocyanins were absent. Transcripts of the MBW complex (anthocyanin2, MYC, and WD40), which regulates the biosynthesis of anthocyanins, were present in the leaves of all cultivars with a maximum in the purple leaves of the cv. Samotsvet. Comparison of biochemical and expression data revealed a positive correlation between the amount of anthocyanins in fruit peel and leaves and UFGT1 expression level. For UFGT2 such correlation was no found. Analysis of UFGT1 sequence, including the promoter region, in 18 pepper cultivars that differ in fruit color pattern, revealed sequence invariance, regardless of the color of the immature fruit. Analysis of the UFGT1 and UFGT2 promoter sequences of the showed differences in the composition of cis-regulatory elements involved in response to stress and hormones, and in MYB and MYC transcription factors binding sites.

Keywords

Capsicum spp., pepper cultivars, anthocyanins biosynthesis, anthocyanidin-3-O-glucosyltransferase, UFGT, the content of anthocyanins, gene expression.

References

Mateos R.M., Jiménez A., Román P. et al. Antioxidant systems from pepper (Capsicum annuum L.): Involvement in the response to temperature changes in ripe fruits // Int. J. Mol. Sci. 2013. V.14. P. 9556–9580 https://doi.org/10.3390/ijms14059556
Moscone E.A., Scaldaferro M.A., Grabiele M. et al. The evolution of chili peppers (Capsicum – Solanaceae): A cytogenetic perspective // Acta Hortic. 2007. V. 745. P. 137–170. https://doi.org/10.17660/ActaHortic.2007.745.5
García C.C., Barfuss M.H., Sehr E.M. et al. Phylogenetic relationships, diversification and expansion of chili peppers (Capsicum, Solanaceae) // Ann. Bot. 2016. V. 118. № 1. P. 35–51. https://doi.org/10.1093/aob/mcw079
Borovsky Y., Oren-Shamir M., Ovadia R. et al. The A locus that controls anthocyanin accumulation in pepper encodes a MYB transcription factor homologous to Anthocyanin2 of Petunia // Theor. Appl. Genet. 2004. V. 109. P. 23–29. https://doi.org/10.1007/s00122-004-1625-9
Aza-González C., Herrera-Isidrón L., Núñez-Palenius H.G. et al. Anthocyanin accumulation and expression analysis of biosynthesis-related genes during chili pepper fruit development // Biol. Plant. 2013. V. 57. P. 49–55. https://doi.org/10.1007/s10535-012-0265-1
Филюшин М.А., Джос Е.А., Щенникова А.В., Кочиева Е.З. Зависимость окраски плодов перца от соотношения основных пигментов и профиля экспрессии генов биосинтеза каротиноидов и антоцианов // Физиол. растений. 2020. Т. 67. С. 644–653. https://doi.org/10.31857/S0015330320050048
Tanaka Y., Sasaki N., Ohmiya A. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids // Plant J. 2008. V. 54. P. 733–749. https://doi.org/10.1111/j.1365-313X.2008.03447.x
Ma Y., Ma X., Gao X. et al. Light induced regulation pathway of anthocyanin biosynthesis in plants // Int. J. Mol. Sci. 2021. V. 22. https://doi.org/10.3390/ijms222011116
Naing A.H., Kim C.K. Roles of R2R3-MYB transcription factors in transcriptional regulation of anthocyanin biosynthesis in horticultural plants // Plant Mol. Biol. 2018. V. 98. P. 1–18. https://doi.org/10.1007/s11103-018-0771-4
Zhao Z.C., Hu G.B., Hu F.C. et al. The UDP glucose: Flavonoid-3-O-glucosyltransferase (UFGT) gene regulates anthocyanin biosynthesis in litchi (Litchi chinesis Sonn.) during fruit coloration // Mol. Biol. Rep. 2012. V. 6. P. 6409–6415.
Liu Y., Tikunov Y., Schouten R.E. et al. Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: A review // Front. Chem. 2018. V. 6. https://doi.org/10.3389/fchem.2018.00052
Villa-Rivera M.G., Ochoa-Alejo N. Transcriptional regulation of ripening in chili pepper fruits (Capsicum spp.) // Int. J. Mol. Sci. 2021. V. 22. https://doi.org/10.3390/ijms222212151
Филюшин М.А., Джос Е.А., Щенникова А.В., Кочиева Е.З. Особенности экспрессии гена фактора транскрипции anthocyanin2 и его влияния на содержание антоцианов у образцов Capsicum chinense Jacq. с различной окраской плода // Генетика. 2020. Т. 56. С. 1161–1170. https://doi.org/10.31857/S0016675820090064
Wang Y., Liu S., Wang H. et al. Identification of the regulatory genes of UV-B-induced anthocyanin biosynthesis in pepper fruit // Int. J. Mol. Sci. 2022. V. 23. https://doi.org/10.3390/ijms23041960
Liu J., Ai X., Wang Y. et al. Fine mapping of the Ca3GT gene controlling anthocyanin biosynthesis in mature unripe fruit of Capsicum annuum L. // Theor. Appl. Genet. 2020. V. 133(9). P. 2729–2742. https://doi.org/10.1007/s00122-020-03628-7
Kobayashi S., Yamamoto N.G., Hirochika H. Association of VvmybA1 gene expression with anthocyanin production in grape (Vitis vinifera) skin – color mutants // J. Jpn. Soc. Hortic. Sci. 2005. V. 74. P. 196–203.
Solovchenko A.E., Chivkunova O.B., Merzlyak M.N., Reshetnikova I.V. A spectrophotometric analysis of pigments in apples // Rus. J. Plant Phys. 2001. V. 48. № 5. P. 693–700.
Cappellini F., Marinelli A., Toccaceli M. et al. Anthocyanins: From mechanisms of regulation in plants to health benefits in foods // Front. Plant Sci. 2021. V. 12. https://doi.org/10.3389/fpls.2021.748049
Cui Z.H., Bi W.L., Hao X.Y. et al. Drought stress enhances up-regulation of anthocyanin biosynthesis in grapevine leafroll-associated virus 3-infected in vitro grapevine (Vitis vinifera) leaves // Plant Dis. 2017. V. 101(9). P. 1606–1615. https://doi.org/10.1094/PDIS-01-17-0104-RE
Sicilia A., Catara V., Scialò E., Lo Piero A.R. Fungal infection induces anthocyanin biosynthesis and changes in DNA methylation configuration of blood orange [Citrus sinensis L. (Osbeck)] // Plants (Basel). 2021. V. 10(2). https://doi.org/10.3390/plants10020244
Gutha L.R., Casassa L.F., Harbertson J.F., Naidu R.A. Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves // BMC Plant Biol. 2010. V. 10. https://doi.org/10.1186/1471-2229-10-187