VvMYB14 participates in melatonin-induced proanthocyanidin biosynthesis by upregulating expression of VvMYBPA1 and VvMYBPA2 in grape seeds

Xiaoqian Zhang , Wanyun Ma , Xueqiang Guan , Fei Wang , Zongbao Fan , Shiwei Gao , Yuxin Yao

Horticulture Research ›› 2023, Vol. 10 ›› Issue (2) : 274

PDF (2363KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (2) :274 DOI: 10.1093/hr/uhac274
Article
research-article
VvMYB14 participates in melatonin-induced proanthocyanidin biosynthesis by upregulating expression of VvMYBPA1 and VvMYBPA2 in grape seeds
Author information +
History +
PDF (2363KB)

Abstract

This work demonstrated that melatonin increases continuously in seeds, particularly seed coats, during berry ripening. Exogenous melatonin treatments significantly increased the proanthocyanidin (PA) content, partially through ethylene signaling, in seed coats. VvMYB14 expression exhibited patterns similar to melatonin accumulation over time, which was largely induced by melatonin treatment in seed coats during berry ripening. Additionally, VvMYB14 bound to the MBS element of the VvMYBPA1 promoter to activate expression. VvMYB14 overexpression largely upregulated expression of VvMYBPA1, VvMYBPA2 and VvLAR1 and increased the PA content in grape seed-derived calli. Similar increases in AtTT2 and AtBAN expression and PA content were found in VvMYB14-overexpressing Arabidopsis seeds. It was also observed that VvMYB14 overexpression increased ethylene production and thereby induced expression of VvERF104, which bound to the ERF element of the VvMYBPA2 promoter and activated its expression. Additionally, VvERF104 suppression reduced the VvMYB14 overexpression-induced increases in expression of VvMYBPA2 and VvLAR1 and PA content. Further experiments revealed that melatonin-induced increases in the expression of VvMYBPA1, VvMYBPA2, VvERF104 and VvLAR1 and PA accumulation were significantly reduced in VvMYB14-suppressing grape calli and leaves. Collectively, VvMYB14 mediates melatonin-induced PA biosynthesis by directly transactivating VvMYBPA1 expression and indirectly upregulating VvMYBPA2 expression via VvERF104.

Cite this article

Download citation ▾
Xiaoqian Zhang, Wanyun Ma, Xueqiang Guan, Fei Wang, Zongbao Fan, Shiwei Gao, Yuxin Yao. VvMYB14 participates in melatonin-induced proanthocyanidin biosynthesis by upregulating expression of VvMYBPA1 and VvMYBPA2 in grape seeds. Horticulture Research, 2023, 10 (2) : 274 DOI:10.1093/hr/uhac274

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This study was financially supported by National Key R&D Program of China (2018YFD1000200), Agriculture Improved Variety Project of Shandong Province (2020LZGC008), Major Project of Science and Technology of Shandong Province (2022CXGC010605), Fruit Industrial Technology System of Shandong Province (SDAIT-06-03) and the National Natural Science Foundation of China (31872068 and 32072537).

Author contributions

Y.Y. and X.Z. conceived and designed the research; X.Z., W.M., F.W. and Z.F. performed the experiments; X.G. and S.G. analyzed the data; and Y.Y. wrote the manuscript. All authors read and approved the manuscript.

Data availability

All the experimental data are available and accessible via the main text and/or the supplemental data.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

[1]

Dixon RA, Xie DY, Sharma SB . Proanthocyanidins-a final frontier in flavonoid research? New Phytol 2005; 165: 9-28.

[2]

Liu C, Wang X, Shulaev V et al. A role for leucoanthocyanidin reductase in the extension of proanthocyanidins. Nat Plants 2016; 2: 16182.

[3]

Hanlin R, Kelm M, Wilkinson K et al. Detailed characterization of proanthocyanidins in skin, seeds, and wine of shiraz and cabernet sauvignon wine grapes (Vitis vinifera). J Agric Food Chem 2011; 59: 13265-76.

[4]

Xie DY, Sharma SB, Paiva NL et al. Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 2003; 299: 396-9.

[5]

Yu KJ, Jun JH, Duan CQ et al. VvLAR1 and VvLAR2 are bifunctional enzymes for proanthocyanidin biosynthesis in grapevine. Plant Physiol 2019; 180: 1362-74.

[6]

Bogs J, Jaffé FW, Takos AM et al. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 2007; 143: 1347-61.

[7]

Terrier N, Torregrosa L, Ageorges À et al. Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 2009; 149: 1028-41.

[8]

Galano A, Tan DX, Reiter RJ . Melatonin as a naturalally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.

[9]

Arnao MB, Hernándezruiz J . Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 2019; 24: 38-48.

[10]

Sun Q, Zhang N, Wang J et al. Melatonin promotes ripening and improves quality of tomato fruit during postharvest life. J Exp Bot 2015; 66: 657-68.

[11]

Xu L, Yue Q, Bian F’ et al. Melatonin enhances phenolics accumulation partially via ethylene signaling and resulted in high antioxidant capacity in grape berries. Front Plant Sci 2017; 8: 1426.

[12]

Hu W, Yang H, Tie W et al. Natural variation in banana varieties highlights the role of melatonin in postharvest ripening and quality. J Agr Food Chem 2017; 65: 9987-94.

[13]

Liu J, Yue R, Si M et al. Effects of exogenous application of melatonin on quality and sugar metabolism in ‘Zaosu’ pear fruit. J Plant Growth Regul 2019; 38: 1161-9.

[14]

Aghdam MS, Fard JR . Melatonin treatment attenuates postharvest decay and maintains nutritional quality of strawberry fruits (Fragaria× anannasa cv. Selva) by enhancing GABA shunt activity . Food Chem 2017; 221: 1650-7.

[15]

Ma WY, Xu L, Gao S et al. Melatonin alters the secondary metabolite profile of grape berry skin by promoting VvMYB14-mediated ethylene biosynthesis . Hortic Res 2021; 8: 43.

[16]

Höll J, Vannozzi A, Czemmel S et al. The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 2013; 25: 4135-49.

[17]

Xu L, Yue Q, Xiang G et al. Melatonin promotes ripening of grape berry via increasing the levels of ABA, H2O2, and particularly ethylene . Hortic Res 2018; 5: 1-11.

[18]

Liu CG, Jun JH, Dixon RA . MYB5 and MYB14 play pivotal roles in seed coat polymer biosynthesis in Medicago truncatula. Plant Physiol 2014; 165: 1424-39.

[19]

Xu WJ, Dubos C, Lepiniec L . Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 2015; 20: 176-85.

[20]

Wan DY, Guo Y, Cheng Y et al. CRISPR/Cas9-mediated mutagenesis of VvMLO3 results in enhanced resistance to powdery mildew in grapevine (Vitis vinifera). Hortic Res 2020; 7: 116.

[21]

Tanner GJ, Francki KT, Abrahams S et al. Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. J Biol Chem 2003; 278: 31647-56.

[22]

Nesi N, Jond C, Debeaujon I et al. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed . Plant Cell 2001; 13: 2099-114.

[23]

Zimmermann IM, Heim MA, Weisshaar B et al. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins . Plant J 2004; 40: 22-34.

[24]

Gargouri M, Chaudière J, Manigand C et al. The epimerase activity of anthocyanidin reductase from Vitis vinifera and its regiospecific hydride transfers . Biol Chem 2010; 391: 219-27.

[25]

Peng QZ, Zhu Y, Liu Z et al. An integrated approach to demonstrating the ANR pathway of proanthocyanidin biosynthesis in plants. Planta 2012; 236: 901-18.

[26]

Bellincontro A, Fardelli A, Santis DD et al. Postharvest ethylene and 1-MCP treatments both affect phenols, anthocyanins, and aromatic quality of Aleatico grapes and wine. Aust J Grape Wine Res 2006; 12: 141-9.

[27]

Xu LL, Xiang G, Sun Q et al. Melatonin enhances salt tolerance by promoting MYB108A-mediated ethylene biosynthesis in grapevines . Hortic Res 2019; 6: 114.

[28]

Sun L, Zhang M, Ren J et al. Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biol 2010; 10: 257-67.

[29]

Zhang J, Xu H, Wang N et al. The ethylene response factor MdERF1B regulates anthocyanin and proanthocyanidin biosynthesis in apple. Plant Mol Biol 2018; 98: 205-18.

[30]

Bethke G, Unthan T, Uhrig JF et al. Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling . PNAS 2009; 106: 8067-72.

[31]

Czemmel S, Heppel SC, Bogs J . R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 2012; 249: 109-18.

[32]

Xiao QL, Wang Y, Du J et al. ZmMYB14 is an important transcription factor involved in the regulation of the activity of the ZmBT1 promoter in starch biosynthesis in maize . FEBS J 2017; 284: 3079-99.

[33]

Shelton D, Stranne M, Mikkelsen L et al. Transcription factors of lotus: regulation of isoflavonoid biosynthesis requires coordinated changes in transcription factor activity. Plant Physiol 2012; 159: 531-47.

[34]

Sharma SB, Dixon RA . Metabolic engineering of proanthocyanidins by ectopic expression of transcription factors in Arabidopsis thaliana. Plant J 2005; 44: 62-75.

[35]

Kong XP, Li C, Zhang F et al. Ethylene promotes cadmium-induced root growth inhibition through EIN3 controlled XTH33 and LSU1 expression in Arabidopsis. Plant Cell Environ 2018; 41: 2449-62.

[36]

Feucht W, Polster J . Nuclei of plants as a sink for flavanols. Z Naturforsch 2001; 56: 479-82.

[37]

Yue QY, Xu LL, Xiang GQ et al. Characterization of gene expression profile, phenolic composition and antioxidant capacity in red-fleshed grape berries and their wines. J Agric Food Chem 2018; 66: 7190-9.

[38]

Sun B, Ricardo-da-Silva JM, Spranger I . Critical factors of vanillin assay for catechins and proanthocyanidins. J Agric Food Chem 1998; 46: 4267-74.

[39]

Tucker ML, Xue P, Yang R . 1-Aminocyclopropane-1-carboxylic acid (ACC) concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode (Heterodera glycines)-infected roots . J Exp Bot 2010; 61: 463-72.

[40]

Yang Y, Li R, Qi M . In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves . Plant J 2000; 22: 543-51.

[41]

Jefferson RA, Kavanagh TA, Bevan MW . GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 1987; 6: 3901-7.

[42]

Guo H, Guo H, Zhang L et al. Metabolome and transcriptome association analysis reveals dynamic regulation of purine metabolism and flavonoid synthesis in transdifferentiation during somatic embryogenesis in cotton. Int J Mol Sci 2019; 20: 2070.

[43]

Clough SJ, Bent AF . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998; 16: 735-43.

PDF (2363KB)

85

Accesses

0

Citation

Detail

Sections
Recommended

/