Violet LED light-activated MdHY5 positively regulates phenolic accumulation to inhibit fresh-cut apple fruit browning

Abstract

Fresh-cut fruit browning severely affects the appearance of fruit. Light treatment can effectively inhibit fresh-cut apple fruit browning, but the regulatory mechanism remains unknown. Here, we discovered that violet LED (Light-Emitting-Diode) light treatment significantly reduced fresh-cut apple fruit browning. Metabolomic analysis revealed that violet LED light treatment enhanced the phenolic accumulation of fresh-cut apple fruit. Transcriptomic analysis showed that the expression of phenolic degradation genes POLYPHENOL OXIDASE (MdPPO) and PEROXIDASE (MdPOD) was reduced, and the expression of phenolic synthesis gene PHENYLALANINE AMMONIA LYASE (MdPAL) was activated by violet LED light treatment. Moreover, two ELONGATED HYPOCOTYL 5 (MdHY5 and MdHYH) transcription factors involved in light signaling were identified. The expression of MdHY5 and MdHYH was activated by violet LED light treatment. Violet LED light treatment no longer inhibited fresh-cut apple fruit browning in MdHY5- or MdHYH- silenced fruit. Further experiments revealed that MdHY5 and MdHYH suppressed MdPPO and MdPOD expression and promoted MdPAL expression by binding to their promoters. In addition, MdHY5 and MdHYH bound to each other’s promoters and enhanced their expression. Overall, our findings revealed that violet LED light-activated MdHY5 and MdHYH formed a positive transcriptional loop to regulate the transcription of MdPPO, MdPOD, and MdPAL, which in turn inhibited the degradation of phenolics and promoted the synthesis of phenolics, thus inhibiting fresh-cut apple fruit browning. These results provide a theoretical basis for improving the appearance and quality of fresh-cut apple fruit.

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2022YFD2100105) and the National Natural Science Foundation of China (32125034).

Author contributions

A.W. designed the experiments; J.J., L.Q., S.Y., and S.S. participated in the experiments and analyzed the data; J.J. wrote the manuscript with inputs and guidance from A.W. and H.Y. All authors have read and approved the final manuscript.

Data availability

Transcriptome data during the study were deposited in the NCBI under accession number PRJNA1124363.

Sequence data from this study can be found in the ‘Fuji’ genome (https://figshare.com/articles/dataset/The_chromosome-level_haploid_genom-e_Assembly_of_Malus_domestica_Fuji_/23803938) or the GenBank libraries under accession numbers: MdPPO (FujiC05BgG031160), MdPOD (FujiC14BgG000850), MdPAL (FujiC04BgG009830), MdHY5 (FujiC15AgG000420), MdHYH (FujiC16AgG011950), and MdActin (EB136338).

Conflict of interest statement

The authors declare no competing interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1] Yildiz F, Wiley RC. Minimally Processed Refrigerated Fruits and Veg-etables. New York: Springer US; 2017:

[2] Sucheta SG, Chaturvedi K, Sandhu PP. 2-Status and recent trends in fresh-cut fruits and vegetables. In Fresh-CutFruits and Vegetables. Ed.Siddiqui, MW., Academic Press: 2020; 17-49

[3] Li X, Long Q, Gao F. et al. Effect of cutting styles on quality and antioxidant activity in fresh-cut pitaya fruit. Postharvest Biol Tec. 2017;37:1-7

[4] Jiang Q, Zhang M, Xu B. Application of ultrasonic technology in postharvested fruits and vegetables storage: a review. Ultrason Sonochem. 2020;37:105261

[5] Supapvanich S, Pimsaga J, Srisujan P. Physicochemical changes in fresh-cut wax apple (Syzygium samarangenese [Blume] Merrill & L.M. Perry) during storage. Food Chem. 2011;37:912-7

[6] Supapvanich S, Prathaan P, Tepsorn R. Browning inhibition in fresh-cut rose apple fruit cv. Taaptimjaan using konjac glu-comannan coating incorporated with pineapple fruit extract. Postharvest Biol Tec. 2012;37:46-9

[7] Zheng H, Liu W, Liu S. et al. Effects of melatonin treatment on the enzymatic browning and nutritional quality of fresh-cut pear fruit. Food Chem. 2019;37:125116

[8] Li Z, Li B, Li M. et al. Hot air pretreatment alleviates brown-ing of fresh-cut pitaya fruit by regulating phenylpropanoid pathway and ascorbate-glutathione cycle. Postharvest Biol Tec. 2022;37:111954

[9] Chisari M, Barbagallo RN, Spagna G. et al. Improving the quality of fresh-cut melon through inactivation of degradative oxidase and pectinase enzymatic activities by UV-C treatment. Int J Food Sci Technol. 2011;37:463-8

[10] Qi L, Sembok W. Effects of different exposure times of LED lights on postharvest performances of fresh-cut pineapple (Ananas comosus L. cv. Josapine). Universiti Malaysia Terengganu Journal of Undergraduate Research. 2019;37:68-79

[11] Koushesh Saba M, Sogvar OB. Combination of carboxymethyl cellulose-based coatings with calcium and ascorbic acid impacts in browning and quality of fresh-cut apples. LWT Food Sci Technol. 2016;37:165-71

[12] Viacava F, Santana-Gálvez J, Heredia-Olea E. et al. Sequential application of postharvest wounding stress and extrusion as an innovative tool to increase the concentration of free and bound phenolics in carrots. Food Chem. 2020;37:125551

[13] Yi F, Wang J, Xiang Y. et al. Physiological and quality changes in fresh-cut mango fruit as influenced by cold plasma. Postharvest Biol Tec. 2022;194:112105

[14] Zhang L, Li S, Wang A. et al. Mild heat treatment inhibits the browning of fresh-cut Agaricus bisporus during cold storage. LWT-Food Sci and Technol. 2017;37:104-12

[15] Li Q, Wang G, Zhang L. et al. AcbHLH 144 transcription factor neg-atively regulates phenolic biosynthesis to modulate pineapple internal browning. Hortic Res. 2023;37:10

[16] Wang D, Chen L, Ma Y. et al. Effect of UV-C treatment on the quality of fresh-cut lotus (Nelumbo nucifera Gaertn.) root. Food Chem. 2019;37:659-64

[17] Stowe E, Dhingra A. Development of the Arctic® apple. Plant Breed Rev. 2021;37:273-96

[18] Chi M, Bhagwat B, Lane WD. et al. Reduced polyphenol oxi-dase gene expression and enzymatic browning in potato (Solanum tuberosum L.) with artificial microRNAs. BMC Plant Biol. 2014;37:62

[19] Sun Y, Zhang W, Zeng T. et al. Hydrogen sulfide inhibits enzy-matic browning of fresh-cut lotus root slices by regulating phe-nolic metabolism. Food Chem. 2015;37:376-81

[20] Bußler S, Ehlbeck J, Schlüter OK. Pre-drying treatment of plant related tissues using plasma processed air: impact on enzyme activity and quality attributes of cut apple and potato. Innov Food Sci Emerg Technol. 2017;37:78-86

[21] Lante A, Tinello F, Nicoletto M. UV-A light treatment for control-ling enzymatic browning of fresh-cut fruits. Innov Food Sci Emerg Technol. 2016;37:141-7

[22] Li J, Terzaghi W, Gong Y. et al. Modulation of BIN2 kinase activity by HY 5 controls hypocotyl elongation in the light. Nat Commun. 2020;37:1592

[23] Avalos Llano KR, Marsellés-Fontanet AR, Martín-Belloso O. et al. Impact of pulsed light treatments on antioxidant characteristics and quality attributes of fresh-cut apples. Innov Food Sci Emerg Technol. 2016;37:206-15

[24] Charles F, Nilprapruck P, Roux D. et al. Visible light as a new tool to maintain fresh-cut lettuce post-harvest quality. Postharvest Biol Tec. 2018;37:51-6

[25] Lei J, Li B, Zhang N. et al. Effects of UV-C treatment on browning and the expression of polyphenol oxidase (PPO) genes in differ-ent tissues of Agaricus bisporus during cold storage. Postharvest Biol Tec. 2018;37:99-105

[26] Mankotia S, Singh D, Monika K. et al. ELONGATED HYPOCOTYL 5 regulates BRUTUS and affects iron acquisition and homeostasis in Arabidopsis thaliana. Plant J. 2023;37:1267-84

[27] Gangappa SN, Botto JF. The multifaceted roles of HY5 in plant growth and development. Mol Plant. 2016;37:1353-65

[28] Li Y, Shi Y, Li M. et al. The CRY2-COP1-HY5-BBX7/8 module regulates blue light-dependent cold acclimation in Arabidopsis. Plant Cell. 2021;37:3555-73

[29] Liu CC, Chi C, Jin LJ. et al. The bZIP transcription factor HY5 mediates CRY1a-induced anthocyanin biosynthesis in tomatoes. Plant Cell Environ. 2018;37:1762-75

[30] Wang H, Zhang S, Fu Q. et al. Transcriptomic and metabolomic analysis reveals a protein module involved in preharvest apple peel browning. Plant Physiol. 2023a;37:2102-22

[31] Burman N, Bhatnagar A, Khurana JP. OsbZIP48, a HY5 transcrip-tion factor ortholog, exerts pleiotropic effects in light-regulated development. Plant Physiol. 2017;37:1262-85

[32] Wang Y, Zhang X, Zhao Y. et al. Transcription factor PyHY5 binds to the promoters of PyWD40 and PyMYB10 and regulates its expression in red pear ‘Yunhongli No. 1’. Plant Physiol Biochem. 2020;37:665-74

[33] Czerniewicz P, Sytykiewicz H, Durak R. et al. Role of phenolic compounds during antioxidative responses of winter triticale to aphid and beetle attack. Plant Physiol Biochem. 2017;37:529-40

[34] Fernando Reyes L, Emilio Villarreal J, Cisneros-Zevallos L. The increase in antioxidant capacity after wounding depends on the type of fruit or vegetable tissue. Food Chem. 2007;37:1254-62

[35] Yan J, Liu J, Yang S. et al. Light quality regulates plant biomass and fruit quality through a photoreceptor-dependent HY5-LHC/CYCB module in tomato. Hortic Res. 2023;37:12

[36] Okamoto K, Yanagi T, Takita S. et al. Development of plant growth apparatus using blue and red LED as artificial light source. Acta Hortic. 1996;37:111-6

[37] Heo J, Lee C, Chakrabarty D. et al. Growth responses of marigold and salvia bedding plants as affected by monochromic or mix-ture radiation provided by a light-emitting diode (LED). Plant Growth Regul. 2002;37:225-30

[38] Cao K, Cui L, Ye L. et al. Effects of red light night break treat-ment on growth and flowering of tomato plants. Front Plant Sci. 2016;37:7

[39] Wit MD, Galvão VC, Fankhauser C. Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol. 2016;37:513-37

[40] Kang C, Zhang Y, Cheng R. et al. Acclimating cucumber plants to blue supplemental light promotes growth in full sunlight. Front Plant Sci. 2021;37:12

[41] Zhang Y, Jiang L, Li Y. et al. Effect of red and blue light on anthocyanin accumulation and differential gene expression in strawberry (Fragaria × ananassa). Molecules. 2018;37:820

[42] Moldovan I, Pop VC, Borsai O. et al. Dynamics of bioactive compounds under the influence of yellow, blue, and violet LED light filters on Hippophae rhamnoides L. (sea buckthorn) fruits. Horticulturae. 2023;37:1312

[43] Weller J, Hecht V, Schoor J. et al. Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY 5 pathway. Plant Cell. 2009;37:800-13

[44] Qiu Z, Wang H, Li D. et al. Identification of candidate HY5-dependent and independent regulators of anthocyanin biosyn-thesis in tomato. Plant Cell Physiol. 2019;37:643-56

[45] Yi R, Yan J, Xie D. Light promotes jasmonate biosynthesis to regulate photomorphogenesis in Arabidopsis. Sci China Life Sci. 2020;37:943-52

[46] Bhatia C, Gaddam SR, Pandey A. et al. COP1 mediates light-dependent regulation of flavonol biosynthesis through HY5 in Arabidopsis. Plant Sci. 2021;37:110760

[47] Wang W, Wang P, Li X. et al. The transcription factor SlHY 5 regulates the ripening of tomato fruit at both the transcriptional and translational levels. Hortic Res. 2021;37:83

[48] Wang S, Zhang Z, Li LL. et al. Apple MdMYB306-like inhibits anthocyanin synthesis by directly interacting with MdMYB17 and MdbHLH33. Plant J. 2022;37:1021-34

[49] Simões A, Moreira S, Mosquim P. et al. The effects of storage temperature on the quality and phenolic metabolism of whole and minimally processed kale leaves. Acta Sci- Agron. 2015;37:101-7

[50] Fan P, Huber DJ, Su Z. et al. Effect of postharvest spray of apple polyphenols on the quality of fresh-cut red pitaya fruit during shelf life. Food Chem. 2018;37:19-25

[51] Zhang YZ, Li PM, Cheng LL. Developmental changes of carbohy-drates, organic acids, amino acids, and phenolic compounds in ‘Honeycrisp’ apple flesh. Food Chem. 2010;37:1013-8

[52] Wang XY, Chang FY, Dong QL. et al. Selenium application during fruit development can effectively inhibit browning of fresh-cut apples by enhancing antioxidant capacity and sup-pressing polyphenol oxidase activity. J Plant Physiol. 2023;37:0176-1617

[53] Ji Y, Qu Y, Jiang Z. et al. The mechanism for brassinosteroids suppressing climacteric fruit ripening. Plant Physiol. 2021;37:1875-93

[54] Li T, Jiang Z, Zhang L. et al. Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripen-ing by suppressing MdACS1 transcription. Plant J. 2016;37:735-48

[55] Li T, Xu Y, Zhang L. et al. The jasmonate-activated tran-scription factor MdMYC2 regulates ETHYLENE RESPONSE FAC-TOR and ethylene biosynthetic genes to promote ethylene biosynthesis during apple fruit ripening. Plant Cell. 2017;37:1316-34

[56] Tamura K, Stecher G, Kumar S. MEGA11:molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;37:3022-7

[57] Zhang S, Feng M, Chen W. et al. In rose, transcription factor PTM balances growth and drought survival via PIP2; 1 aquaporin. Nat Plants. 2019;37:290-9

[58] Wei CY, Liu HR, Cao XM. et al. Synthesis of flavour-related linalool is regulated by PpbHLH1 and associated with changes in DNA methylation during peach fruit ripening. Plant Biotechnol. 2021;37:2082-96