Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry

Taishan Li , Hisayo Yamane , Ryutaro Tao

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 67

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :67 DOI: 10.1038/s41438-021-00503-4
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Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry
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Abstract

Ultraviolet-B (UV-B) light (280–315 nm) is an important environmental signal that regulates plant development and photomorphogenesis, while also affecting the flavonoid pathway, including anthocyanin biosynthesis. Regarding the effects of UV-B radiation on fruits, the effects of a short-term or postharvest irradiation on fruit quality have been well-documented, but the effects of a long-term preharvest UV-B irradiation on fruit growth and coloration remain unclear. Thus, in this study, we investigated the effects of a long-term treatment involving an environmentally relevant UV-B dose on highbush blueberry ( Vaccinium corymbosum) fruit. The preharvest UV-B treatment quickly promoted fruit growth and sugar accumulation, which is not commonly observed in other fruit tree species. The UV-B exposure also accelerated fruit ripening and coloration. The dual-luciferase assay proved that in blueberries, expression of VcUFGT encoding anthocyanin biosynthesis key enzyme, is positively and negatively regulated by VcMYBA1 and VcMYBC2, respectively. Throughout the fruit development stage, the UV-B treatment up-regulated VcMYBPA1 expression, which increased VcUFGT expression via VcMYBA1. In the green fruit stage, the UV-B treatment increased HY5 encoding UV receptor, which up-regulates VcMYBPA1 and down-regulates VcMYBC2, thereby promotes the accumulation of anthocyanins. On the other hand, excessive anthocyanin synthesis was inhibited by increased VcMYBC2 levels in mature fruits when exposed to UV-B light through HY5-independent pathway. In conclusion, anthocyanin-related MYB activators and repressor may coordinately balance the accumulation of anthocyanins in blueberry fruits, with UV-B treatments possibly influencing their effects in a stage-specific manner. The potential utility of preharvest UV-B treatments for improving blueberry fruit quality is discussed herein.

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Taishan Li, Hisayo Yamane, Ryutaro Tao. Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry. Horticulture Research, 2021, 8 (1) : 67 DOI:10.1038/s41438-021-00503-4

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References

[1]

Bassman, J. H. Ecosystem consequences of enhanced solar ultraviolet radiation: Secondary plant metabolites as mediators of multiple trophic interactions in terrestrial plant communities. Photochem. Photobiol. 79, 382-398 (2004).

[2]

Kalt, W. et al. Recent research on the health benefits of blueberries and their anthocyanins. Adv. Nutr. 11, 224-236 (2020).

[3]

Li, Y., Sun, H. & Chen, L. The blueberry industry of China: the past 10 years and the future. Acta Hortic 1180, 531-536 (2016).

[4]

Muñoz, P. et al. Comparing the environmental impacts of greenhouse versus open-field tomato production in the Mediterranean region. Acta Hortic 801, 1591-1596 (2008).

[5]

Dzakovich, M. P., Ferruzzi, M. G. & Mitchell, C. A. Manipulating sensory and phytochemical profiles of greenhouse tomatoes using environmentally relevant doses of ultraviolet radiation. J. Agric. Food Chem. 64, 6801-6808 (2016).

[6]

Norberto, S. et al. Blueberry anthocyanins in health promotion: a metabolic overview. J. Funct. Foods 5, 1518-1528 (2013).

[7]

Sun, T. et al. VvVHP1; 2 is transcriptionally activated by VvMYBA1 and promotes anthocyanin accumulation of grape berry skins via glucose signal. Front. Plant Sci. 8, 1811 (2017).

[8]

Henry-Kirk, R. A. et al. Solar UV light regulates flavonoid metabolism in apple (Malus x domestica). Plant Cell Environ. 41, 675-688 (2018).

[9]

Josuttis, M. et al. Solar UVB response of bioactives in strawberry (Fragaria× ananassa Duch. L.): a comparison of protected and open-field cultivation. J. Agric. Food Chem. 58, 12692-12702 (2010).

[10]

Nguyen, C. T., Lim, S., Lee, J. G. & Lee, E. J. VcBBX, VcMYB21, and VcR2R3MYB transcription factors are involved in UV-B-induced anthocyanin biosynthesis in the peel of harvested blueberry fruit. J. Agric. Food Chem. 65, 2066-2073 (2017).

[11]

Yang, J. et al. Transcriptional activation of anthocyanin biosynthesis in developing fruit of blueberries (Vaccinium corymbosum L.) by preharvest and postharvest UV irradiation. J. Agric. Food Chem. 66, 10931-10942 (2018).

[12]

Yonekura-Sakakibara, K., Higashi, Y. & Nakabayashi, R. The origin and evolution of plant flavonoid metabolism. Front. Plant Sci. 10, 943 (2019).

[13]

Zifkin, M. et al. Gene expression and metabolite profiling of developing highbush blueberry fruit indicates transcriptional regulation of flavonoid metabolism and activation of abscisic acid metabolism. Plant Physiol. 158, 200-224 (2012).

[14]

Colle, M. et al. Haplotype-phased genome and evolution of phytonutrient pathways of tetraploid blueberry. GigaScience 8, giz012 (2019).

[15]

Gupta, V. et al. RNA-Seq analysis and annotation of a draft blueberry genome assembly identifies candidate genes involved in fruit ripening, biosynthesis of bioactive compounds, and stage-specific alternative splicing. Gigascience 4, s13742-015 (2015). -0046-9.

[16]

Lloyd, A. et al. Advances in the MYB-bHLH-WD repeat (MBW) pigment regulatory model: Addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol. 58, 1431-1441 (2017).

[17]

Liu, J., Osbourn, A. & Ma, P. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8, 689-708 (2015).

[18]

Cavallini, E. et al. The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol. 167, 1448-1470 (2015).

[19]

Zhou, H. et al. Activator-type R2R3-MYB genes induce a repressor-type R2R3-MYB gene to balance anthocyanin and proanthocyanidin accumulation. N. Phytologist 221, 1919-1934 (2019).

[20]

Plunkett, B. J. et al. MYBA from blueberry (Vaccinium section Cyanococcus) is a subgroup 6 type R2R3MYB transcription factor that activates anthocyanin production. Front. Plant Sci. 9, 1300 (2018).

[21]

Günther, C. S. et al. Spatiotemporal modulation of flavonoid metabolism in blueberries. Front. Plant Sci. 11, 545 (2020).

[22]

Yin, R. & Ulm, R. How plants cope with UV-B: from perception to response. Curr. Opin. Plant Biol. 37, 42-48 (2017).

[23]

Inostroza-Blancheteau, C. et al. Effects of UV-B radiation on anatomical characteristics, phenolic compounds and gene expression of the phenylpropanoid pathway in highbush blueberry leaves. Plant Physiol. Biochem. 85, 85-95 (2014).

[24]

Caldwell, M. M. et al. Effects of increased solar ultraviolet radiation on terrestrial plants. Ambio 24, 166-173 (1995).

[25]

Yu, K. et al. Methods for RNA isolation from blueberry tissues. J. Zhejiang Norm. Univ. (Nat. Sci.) 39, 60-64 (2016).

[26]

Dereeper, A. et al. Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469 (2008).

[27]

Irizumi, J. et al. Analysis of antioxidant capacity and anthocyanin composition among the cultivars of blueberry (Vaccinium spp.). Bull. Fac. Agriculture, Kagoshima. Univ. 63, 27-38 (2013). (In Japanese with English summary).

[28]

Bai, S. et al. BBX16, a B-box protein, positively regulates light-induced anthocyanin accumulation by activating MYB10 in red pear. Plant Biotechnol. J. 17, 1985-1997 (2019).

[29]

Li, J. et al. PpCBFs selectively regulate PpDAMs and contribute to the pear bud endodormancy process. Plant Mol. Biol. 99, 575-586 (2019).

[30]

Higo, K. et al. Plant cis-acting regulatory DNA elements (PLACE) database: 1999 [J]. Nucleic Acids Res. 27, 297-300 (1999).

[31]

Bai, S. et al. Epigenetic regulation of MdMYB1 is associated with paper bagging-induced red pigmentation of apples. Planta 244, 573-586 (2016).

[32]

Bai, S. et al. Two B-box proteins, PpBBX18 and PpBBX21, antagonistically regulate anthocyanin biosynthesis via competitive association with Pyrus pyrifolia ELONGATED HYPOCOTYL 5 in the peel of pear fruit. Plant J. 100, 1208-1223 (2019).

[33]

Zoratti, L. et al. Monochromatic light increases anthocyanin content during fruit development in bilberry. BMC Plant Biol. 14, 377 (2014).

[34]

Burko, Y. et al. Chimeric activators and repressors define HY5 activity and reveal a light-regulated feedback mechanism. Plant Cell 32, 967-983 (2020).

[35]

Kobayashi, S., Ishimaru, M., Ding, C., Yakushiji, H. & Goto, N. Comparison of UDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci. 160, 543-550 (2001).

[36]

Primetta, A. K., Karppinen, K., Riihinen, K. R. & Jaakola, L. Metabolic and molecular analyses of white mutant Vaccinium berries show down-regulation of MYBPA1-type R2R3 MYB regulatory factor. Planta 242, 631-643 (2015).

[37]

Albert, N. W. et al. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26, 962-980 (2014).

[38]

Chen, L., Hu, B., Qin, Y., Hu, G. & Zhao, J. Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol. Biochem. 136, 178-187 (2019).

[39]

Cutanda-Perez, M.-C. et al. Ectopic expression of VlmybA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport. Plant Mol. Biol. 69, 633-648 (2009).

[40]

Terrier, N. et al. Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol. 149, 1028-1041 (2009).

[41]

Loyola, R. et al. 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 (2016).

[42]

Tossi, V., Lamattina, L. & Cassia, R. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. N. Phytologist 181, 871-879 (2009).

[43]

Rakitin, V. Y., Karyagin, V., Rakitina, T. Y., Prudnikova, O. & Vlasov, P. UV-B stress-induced ABA production in Arabidopsis thaliana mutants defective in ethylene signal transduction pathway. Russian J. Plant Physiol. 55, 854-856 (2008).

[44]

Yadukrishnan, P. et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 promotes ABA-mediated inhibition of post germination seedling establishment. Plant J. 103, 481-496 (2020).

[45]

Kossuth, S. & Biggs, R. Ultraviolet radiation affects blueberry fruit quality. Sci. Horticulturae 14, 145-150 (1981).

[46]

Vanhaelewyn, L. et al. Hormone-controlled UV-B responses in plants. J. Exp. Bot. 67, 4469-4482 (2016).

[47]

Wang, X. et al. Ultraviolet B irradiation influences the fruit quality and sucrose metabolism of peach (Prunus persica L.). Environ. Exp. Bot. 153, 286-301 (2018).

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