Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1, and MdMYB17

Shuo Wang , Li-Xian Li , Zhen Zhang , Yue Fang , Dan Li , Xue-Sen Chen , Shou-Qian Feng

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac034

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac034 DOI: 10.1093/hr/uhac034
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Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1, and MdMYB17
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Abstract

Ethylene regulates anthocyanin synthesis in ripening apple fruit via the antagonistic activities of the R2R3-MYB repressors and activators. However, the molecular mechanism underlying this process remains unknown. In this study, ethylene significantly induced the expression of the R2R3-MYB gene MdMYB17 in apple fruit. Moreover, MdMYB17 was revealed to be an important repressor of anthocyanin synthesis. Specifically, MdMYB17 binds directly to the promoters of the ethylene-induced genes MdMYB1 and MdEIL1, which encode positive regulators of anthocyanin synthesis, and represses their expression. Additionally, MdMYB1 and MdEIL1 bind to the MdMYB17 promoter to activate its expression. Thus, MdMYB17, MdMYB1, and MdEIL1 form a regulatory module that controls the expression of the corresponding genes. MdMYB17 interacts with MdEIL1. The interaction between MdMYB17 and MdEIL1 attenuates the regulatory effects of MdMYB17 on MdMYB1 and MdEIL1 as well as the regulatory effects of MdEIL1 on MdMYB17. Overall, our results reveal the molecular mechanisms by which MdMYB17, MdMYB1, and MdEIL1 finely mediate ethylene-regulated anthocyanin synthesis in apple fruit.

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Shuo Wang, Li-Xian Li, Zhen Zhang, Yue Fang, Dan Li, Xue-Sen Chen, Shou-Qian Feng. Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1, and MdMYB17. Horticulture Research, 2022, 9 (1) : uhac034 DOI:10.1093/hr/uhac034

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References

[1]

Cipollini ML, Levey DJ . Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat. 1997; 150: 346-72.

[2]

Gould KS . Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol. 2004; 5: 314-20.

[3]

Schaefer HM, Schaefer V, Levey DJ . How plant-animal interactions signal new insights in communication. Trends Ecol Evol. 2004; 19: 577-84.

[4]

Espley RV, Hellens RP, Jo P et al. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 2007; 49: 414-27.

[5]

Tanaka Y, Sasaki N, Ohmiya A . Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008; 54: 733-49.

[6]

Koes R, Verweij W, Quattrocchio F . Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 2005; 10: 236-42.

[7]

Gonzalez A, Zhao MZ, Leavitt JM et al. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 2008; 53: 814-27.

[8]

Hichri I, Barrieu F, Bogs J et al. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot. 2011; 62: 2465-83.

[9]

Kranz HD, Denekamp M, Greco R et al. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana . Plant J. 1998; 16: 263-76.

[10]

Stracke R, Werber M, Weisshaar B . The R2R3-MYB gene family in Arabidopsis thaliana . Curr Opin Plant Biol. 2001; l4: 447-56.

[11]

Yanhui C, Xiaoyuan Y, Kun H et al. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol. 2006; 60: 107-24.

[12]

Dubos C, Stracke R, Grotewold E et al. MYB transcription factors in Arabidopsis . Trends Plant Sci. 2010; 15: 573-81.

[13]

Liu YH, Lin-Wang K, Espley RV et al. StMYB44 negatively regulates anthocyanin biosynthesis at high temperatures in tuber flesh of potato. J Exp Bot. 2019; 70: 3809-24.

[14]

Chen LH, Hu B, Qin YH et al. Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol Biochem. 2019; 136: 178-87.

[15]

Ban Y, Honda C, Hatsuyama Y et al. Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol. 2007; 48: 958-70.

[16]

Lin-Wang K, Micheletti D, Palmer J et al. High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 2011; 34: 1176-90.

[17]

Xu HF, Wang N, Liu JX et al. The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes. Plant Mol Biol. 2017; 94: 149-65.

[18]

Rubin G, Tohge T, Matsuda F et al. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis . Plant Cell. 2009; 21: 3567-84.

[19]

Takos AM, Jaffé FW, Jacob SR et al. Light induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 2006; 142: 1216-32.

[20]

Whale SK, Singh Z . Endogenous ethylene and color development in the skin of ‘pink lady’ apple. J Am Soc Hortic Sci. 2007; 132: 20-8.

[21]

An XH, Tian Y, Chen KQ et al. MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol. 2015; 56: 650-62.

[22]

An JP, Wang XF, Li YY et al. EIN3-LIKE1, MYB1, and ETHYLENE RESPONSE FACTOR3 act in a regulatory loop that synergistically modulates ethylene biosynthesis and anthocyanin accumulation. Plant Physiol. 2018; 178: 808-23.

[23]

An JP, Wang XF, Zhang XW et al. An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation. Plant Biotechnol J. 2020; 18: 337-53.

[24]

Ni JB, Premathilake AT, Gao YH et al. Ethylene-activated PpERF105 induces the expression of the repressor-type R2R3-MYB gene PpMYB140 to inhibit anthocyanin biosynthesis in red pear fruit. Plant J. 2021; 105: 167-81.

[25]

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

[26]

Giovannoni JJ . Genetic regulation of fruit development and ripening. Plant Cell. 2004; 16: S170-80.

[27]

Wang KL, Li H, Ecker JR . Ethylene biosynthesis and signaling networks. Plant Cell. 2002; 14: S131-51.

[28]

Wang LK, Zhang ZY, Zhang F et al. EIN2-directed histone acetylation requires EIN3-mediated positive feedback regulation in response to ethylene. Plant Cell. 2021; 33: 322-37.

[29]

Espley RV, Leif D, Plunkett B et al. Red to brown: an elevated anthocyanic response in apple drives ethylene to advance maturity and fruit flesh browning. Front Plant Sci. 2019; 10: 1248.

[30]

Zhou H, Lin-Wang K, Wang FR et al. Activator-type R2R3-MYB genes induce a repressor-type R2R3-MYB gene to balance anthocyanin and proanthocyanidin accumulation. New Phytol. 2019; 221: 1919-34.

[31]

Song J, Bangerth F . The effect of harvest date on aroma compound production from ‘Golden Delicious’ apple fruit and relationship to respiration and ethylene production. Postharvest Biol Technol. 1996; 8: 259-69.

[32]

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

[33]

Li T, Xu YX, Zhang LC 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.

[34]

Zhu ZQ, An FY, Feng Y et al. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis . Proc Natl Acad Sci USA. 2011; 108: 12539-44.

[35]

Lingam S, Mohrbacher J, Brumbarova T et al. Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis . Plant Cell. 2011; 23: 1815-29.

[36]

Yao GF, Ming ML, Allan AC et al. Map-based cloning of the pear gene MYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis. Plant J. 2017; 92: 437-51.

[37]

Kagale S, Links MG, Rozwadowski K . Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis . Plant Physiol. 2010; 152: 1109-34.

[38]

Albert NW, Davies KM, Lewis DH et al. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell. 2014; 26: 962-80.

[39]

Wan SZ, Li CF, Ma XD et al. PtrMYb57 contributes to the negative regulation of anthocyanin and proanthocyanidin biosynthesis in poplar. Plant Cell Rep. 2017; 36: 1263-76.

[40]

Jun JH, Liu CG, Xiao XR et al. The transcriptional repressor MYB2 regulates both spatial and temporal patterns of proanthocyandin and anthocyanin pigmentation in Medicago truncatula . Plant Cell. 2015; 27: 2860-79.

[41]

Matsui K, Umemura Y, Ohme-Takagi M . AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis . Plant J. 2008; 55: 954-67.

[42]

Cavallini E, Matus JT, Finezzo L et al. The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol. 2015; 167: 1448-70.

[43]

Salvatierra A, Pimentel P, Moya-León MA et al. Increased accumulation of anthocyanins in Fragaria chiloensis fruits by transient suppression of FcMYB1 gene . Phytochemistry. 2013; 90: 25-36.

[44]

Jeong SW, Das PK, Jeoung SC et al. Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis . Plant Physiol. 2010; 154: 1514-31.

[45]

Bi SQ, An JP, Wang XF et al. Ethylene response factor MdERF3 promotes anthocyanin and proanthocyanidin accumulation in apple. Acta Horticulturae Sinica. 2019; 46: 2277-85.

[46]

Yang T, Ma HY, Li Y et al. Apple MPK4 mediates phosphorylation of MYB1 to enhance light-induced anthocyanin accumulation. Plant J. 2021; 106: 1728-45.

[47]

Ma HY, Yang T, Li Y et al. The long noncoding RNA MdLNC499 bridges MdWRKY1 and MdERF109 function to regulate early-stage light-induced anthocyanin accumulation in apple fruit. Plant Cell. 2021; 33: 3309-30.

[48]

Giusti MM, Wrolstad RE. Characterization and measurement of anthocyanins by UV-visible spectroscopy. In: Wrolstad RE (ed.), Current Protocols in Food Analytical Chemistry.New York: Wiley, 2001, F1.2.1-13.

[49]

Li TZ, Tan DM, Yang X et al. Apple 1-aminocyclopropane-1-carboxylic acid synthase genes, MdACS1 and MdACS3a, are expressed in different systems of ethylene biosynthesis . Plant Mol Biol. 2013; 31: 204-9.

[50]

Feng SQ, Sun SS, Chen XL et al. PyMYB10 and PyMYB10.1 interact with bHLH to enhance anthocyanin accumulation in pears. PLoS One. 2015; 10: e0142112.

[51]

Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001; 25: 402-8.

[52]

Wang N, Qu CZ, Jiang SH et al. The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples. Plant J. 2018; 96: 39-55.

[53]

Dinesh-Kumar SP, Anandalakshmi R, Marathe R et al. Virus-induced gene silencing. Methods Mol Biol. 2003; 236: 287-94.

[54]

Wang N, Xu HF, Jiang SH et al. MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana) . Plant J. 2017; 90: 276-92.

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