Melatonin suppresses ethylene biosynthesis by inhibiting transcription factor MdREM10 during apple fruit ripening

Chen Li , Qian Yu , Yajing Si , Yuling Liang , Shijiao Lin , Guangxin Yang , Weiting Liu , Yinglin Ji , Aide Wang

Horticulture Research ›› 2025, Vol. 12 ›› Issue (5) : 20

PDF (2285KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (5) :20 DOI: 10.1093/hr/uhaf020
Article
research-article
Melatonin suppresses ethylene biosynthesis by inhibiting transcription factor MdREM10 during apple fruit ripening
Author information +
History +
PDF (2285KB)

Abstract

Ethylene, a plant hormone, is essential for apple (Malus domestica) ripening. The precise molecular mechanism by which melatonin (MT) influences ethylene biosynthesis during apple fruit ripening remains unclear. This study found that exogenous MT treatment inhibited ethylene production and postponed apple fruit ripening. The endogenous MT content of apple fruits exhibited an inverse correlation with ethylene production during fruit ripening, suggesting that MT functions as a ripening suppressor in apple fruits. MT treatment suppressed the expression of key ethylene biosynthesis genes, MdACS1 and MdACO1, during apple fruit ripening. MT treatment decreased the expression levels of transcription factors MdREM10 and MdZF32. MdREM10 binds to the MdERF3 promoter, enhancing its expression and subsequently promoting MdACS1 transcription. Furthermore, MdREM10 directly bound to the MdZF32 promoter, promoting its transcription. MdZF32 directly bound to the MdACO1 promoter, inducing its expression. The findings suggested that MT suppresses ethylene biosynthesis and fruit ripening by inhibiting MdREM10, which indirectly promotes MdACS1 transcription via MdERF3 upregulation, and MdACO1 transcription via MdZF32 upregulation.

Cite this article

Download citation ▾
Chen Li, Qian Yu, Yajing Si, Yuling Liang, Shijiao Lin, Guangxin Yang, Weiting Liu, Yinglin Ji, Aide Wang. Melatonin suppresses ethylene biosynthesis by inhibiting transcription factor MdREM10 during apple fruit ripening. Horticulture Research, 2025, 12(5): 20 DOI:10.1093/hr/uhaf020

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This study received funding from the National Key Research and Development Program of China (2022YFD2100105). We thank editage (https://www.editage.cn/) for editing the manuscript.

Author contributions

A.W. and Y.J. conceptualized and planned the study. C.L. and Q.Y. conducted most experiments. Y.S. and S.L. performed protein purification. Y.L. performed the GUS analysis. W.L. and G.Y. created constructs for protein purification. C.L. and Y.J. wrote the article. All authors have approved the final manuscript.

Data availability

The sequence data utilized in this study can be accessed through the Genome Database for Rosaceae (https://www.rosaceae.org) and the apple genome repository at the National Center for Biotechnology Information (NCBI). The sequence accession numbers are: MdREM10 (MD03G1230200), MdZF32 (MD03G1280300), MdERF2 (AB288348), MdERF3 (XM_008339725), MdERF4 (MD03G1231800), MdERF5 (XM008365562), MdACS1 (U89156), MdACO1 (AF030859), MdCOMT1 (XM029104846), MdCOMT2 (NM001434474), and MdActin (EB136338).

Conflict of interest statement

The authors report no conflicts of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Biedrzycka E, Amarowicz R. Diet and health: apple polyphenols as antioxidants. Food Rev Int. 2008;24:235-51

[2]

Tahir II, Johansson E, Olsson ME. Improvement of quality and storability of apple cv. Aroma by adjustment of some pre-harvest conditions. Sci Hortic. 2007;112:164-71

[3]

Costa F, Alba R, Schouten H. et al. Use of homologous and het-erologous gene expression profiling tools to characterize tran-scription dynamics during apple fruit maturation and ripening. BMC Plant Biol. 2010;10:1-17

[4]

Klee HJ, Giovannoni JJ. Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet. 2011;45:41-59

[5]

Ji Y, Wang A. Recent advances in epigenetic triggering of climac-teric fruit ripening. Plant Physiol. 2023;192:1711-7

[6]

Osorio S, Scossa F, Fernie AR. Molecular regulation of fruit ripening. Front Plant Sci. 2013;4:1-8

[7]

Adams DO, Yang SF. Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. P Natl A Sci India B. 1979;76:170-4

[8]

Dandekar AM, Teo G, Defilippi BG. et al. Effect of down-regulation of ethylene biosynthesis on fruit flavor complex in apple fruit. Transgenic Res. 2004;13:373-84

[9]

Schaffer RJ, Friel EN, Souleyre EJF. et al. A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiol. 2007;144:1899-912

[10]

Guo H, Ecker JR. The ethylene signaling pathway: new insights. Curr Opin Plant Biol. 2004;7:40-9

[11]

Chen Y, Etheridge N, Schaller GE. Ethylene signal transduction. Ann Bot. 2005;95:901-15

[12]

Han Y, Kuang J, Chen J. et al. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. 2016;171:1070-84

[13]

Li T, Jiang Z, Zhang L. et al. Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J. 2016;88:735-48

[14]

Ji Y, Xu M, Liu Z. et al. NUCLEOCYTOPLASMIC shuttling of ETHY-LENE RESPONSE FACTOR 5 mediated by nitric oxide suppresses ethylene biosynthesis in apple fruit. New Phytol. 2022;234: 1714-34

[15]

Ireland HS, Yao J, Tomes S. et al. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J. 2013;73: 1044-56

[16]

Zhu M, Chen G, Zhou S. et al. A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol. 2014;55:119-35

[17]

Feng B, Han Y, Xiao Y. et al. The banana fruit Dof transcription factor MaDof23 acts as a repressor and interacts with MaERF9 in regulating ripening-related genes. JExp Bot. 2016;67:2263-75

[18]

Fan Z, Ba L, Shan W. et al. A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6. Plant J. 2018;96:1191-205

[19]

Wang W, Jian W, Wu Y. et al. Genome-wide analysis of coding and non-coding RNA reveals a conserved miR164-NAC regulatory pathway for fruit ripening. New Phytol. 2020b;225:1618-34

[20]

Li T, Zhang X, Wei Y. et al. Comparative transcriptome analysis of the climacteric of apple fruit uncovers the involvement of transcription factors affecting ethylene biosynthesis. Hortic Plant J. 2023;9:659-69

[21]

Lin Z, Hong Y, Yin M. et al. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J. 2008;55:301-10

[22]

Xu L, Xiang G, Sun Q. et al. Melatonin enhances salt toler-ance by promoting MYB108A-mediated ethylene biosynthesis in grapevines. Hortic Res. 2019;6:14

[23]

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

[24]

Yue P, Lu Q, Liu Z. et al. Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening. New Phytol. 2020;226:1781-95

[25]

Li T, Xu Y, Zhang L. et al. The jasmonate-activated transcription factor MdMYC2 regulates ETHYLENE RESPONSE FACTOR and ethylene biosynthetic genes to promote ethylene biosynthesis during apple fruit ripening. Plant Cell. 2017;29:1316-34

[26]

Zhang M, Yuan B, Leng P. The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. JExp Bot. 2009;60: 1579-88

[27]

Ji Y, Qu Y, Jiang Z. et al. The mechanism for brassinosteroids suppressing climacteric fruit ripening. Plant Physiol. 2021;185: 1875-93

[28]

Manit S-T, Jeffrey J, Nutjaree PJ. et al. Serum melatonin levels and antioxidant capacities after consumption of pineapple, orange, or banana by healthy male volunteers. J Pineal Res. 2012;55:58-64

[29]

Nawaz MA, Huang Y, Bie Z. et al. Melatonin: current status and future perspectives in plant science. Front Plant Sci. 2016;6:1230

[30]

Verde A, Míguez JM, Leao-Martins JM. et al. Melatonin con-tent in walnuts and other commercial nuts. Influence of cul-tivar, ripening and processing (roasting). J Food Compos Anal. 2022;105:104180

[31]

Tan D, Hardeland R, Manchester L. et al. Functional roles of mela-tonin in plants, and perspectives in nutritional and agricultural science. JExp Bot. 2012;63:577-97

[32]

Arnao MB, Hernández-Ruiz J. Functions of melatonin in plants: areview. J Pineal Res. 2015;59:133-50

[33]

Mukherjee S. Recent advancements in the mechanism of nitric oxide signaling associated with hydrogen sulfide and melatonin crosstalk during ethylene-induced fruit ripening in plants. Nitric Oxide. 2019;82:25-34

[34]

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;5:41

[35]

Tijero V, Muoz P, Munné-Bosch S. Melatonin as an inhibitor of sweet cherries ripening in orchard trees. Plant Physiol Biochem. 2019;140:88-95

[36]

Mansouri S, Sarikhani H, Sayyari M. et al. Melatonin accelerates strawberry fruit ripening by triggering GAMYB gene expression and promoting ABA accumulation. Sci Hortic. 2021;281:109919

[37]

Okazaki M, Ezura H. Profiling of melatonin in the model tomato (Solanum lycopersicum L.) cultivar micro-tom. J Pineal Res. 2009;46: 338-43

[38]

Zhai R, Liu J, Liu F. et al. Melatonin limited ethylene production, softening and reduced physiology disorder in pear (Pyrus commu-nis L.) fruit during senescence. Postharvest Biol Technol. 2018;139: 38-46

[39]

Onik JC, Wai SC, Li A. et al. Melatonin treatment reduces ethylene production and maintains fruit quality in apple during posthar-vest storage. Food Chem. 2020;337:127753

[40]

Huangfu L, Chen R, Lu Y. et al. OsCOMT, encoding a caffeic acid O-methyltransferase in melatonin biosynthesis, increases rice grain yield through dual regulation of leaf senescence and vascular development. Plant Biotechnol J. 2022;20:1122-39

[41]

Hu Y, Han Z, Sun Y. et al. ERF 4 affects fruit firmness through TPL4 by reducing ethylene production. Plant J. 2020;103: 937-50

[42]

Qiu A, Lei Y, Yang S. et al. CaC3H14 encoding a tandem CCCH zinc finger protein is directly targeted by CaWRKY40 and positively regulates the response of pepper to inoculation by Ralstonia solanacearum. Mol Plant Pathol. 2018;19:2221-35

[43]

Arnao MB, Hernández-Ruiz J. Melatonin and its relationship to plant hormones. Ann Bot. 2018;121:195-207

[44]

Wei W, Tao J, Yin C. et al. Melatonin regulates gene expressions through activating auxin synthesis and signaling pathways. Front Plant Sci. 2022;13:1057993

[45]

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

[46]

Liu J, Yang J, Zhang H. et al. Melatonin inhibits ethylene synthesis via nitric oxide regulation to delay postharvest senescence in pears. J Agric Food Chem. 2019;67:2279-88

[47]

Peng FY, Weselake RJ. Genome-wide identification and anal-ysis of the B3 superfamily of transcription factors in Bras-sicaceae and major crop plants. Theor Appl Genet. 2013;126: 1305-19

[48]

Romanel EC, Schrago CG, Couñago RM. et al. Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS One. 2009;4:e5791

[49]

Matias-Hernandez L, Battaglia R, Galbiati F. et al. VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell. 2010;22:1702-15

[50]

Mantegazza O, Gregis V, Mendes MA. et al. Analysis of the arabidopsis REM gene family predicts functions during flower development. Ann Bot. 2014;114:1507-15

[51]

Caselli F, Beretta VM, Mantegazza O. et al. REM34 and REM35 control female and male gametophyte development in Arabidop-sis thaliana. Front Plant Sci. 2019;10:1351

[52]

Wang Q, Song S, Lu X. et al. Hormone regulation of CCCH zinc finger proteins in plants. Int J Mol Sci. 2022;23:14288

[53]

Xie Z, Yu G, Lei S. et al. CCCH protein-PvCCCH69 acted as a repressor for leaf senescence through suppressing ABA-signaling pathway. Hortic Res. 2021;8:165

[54]

Wang B, Fang R, Chen F. et al. A novel CCCH-type zinc fin-ger protein SAW1 activates OsGA20ox3 to regulate gibberellin homeostasis and anther development in rice. J Integr Plant Biol. 2020a;62:1594-606

[55]

Jan A, Maruyama K, Todaka D. et al. OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tol-erance in rice by regulating stress-related genes. Plant Physiol. 2013;161:1202-16

[56]

Pomeranz MC, Hah C, Lin PC. et al. The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol. 2010;152:151-65

[57]

Tan D, Li T, Wang A. Apple 1-aminocyclopropane-1-aarboxylic acid synthase genes, MdACS1 and MdACS3a, are expressed in different systems of ethylene biosynthesis. Plant Mol Biol Report. 2013;31:204-9

[58]

Li T, Li X, Tan D. et al. Distinct expression profiles of ripening related genes in the ‘Nanguo’ pear (Pyrus ussuriensis) fruits. Sci Hortic. 2014;171:78-82

[59]

Li C, Chen M, Ji M. et al. Transcriptome analysis of ripe peach (Prunus persica) fruit under low-dose UVB radiation. Sci Hortic. 2020a;259:108757

[60]

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;5:290-9

[61]

Li X, Guo W, Li J. et al. Histone acetylation at the promoter for the transcription factor PuWRKY31 affects sucrose accumulation in pear fruit. Plant Physiol. 2020b;182:2035-46

[62]

Huang G, Li T, Li X. et al. Comparative transcriptome anal-ysis of climacteric fruit of Chinese pear (Pyrus ussuriensis) reveals new insights into fruit ripening. PLoS One. 2014;9: e107562

PDF (2285KB)

1114

Accesses

0

Citation

Detail

Sections
Recommended

/