The MdMYB16/MdMYB1-miR7125-MdCCR module regulates the homeostasis between anthocyanin and lignin biosynthesis during light induction in apple.
MdCCR
MdMYB16
miR7125
anthocyanin
apple
light induction
lignin
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
23
12
2020
accepted:
19
04
2021
pubmed:
29
4
2021
medline:
13
7
2021
entrez:
28
4
2021
Statut:
ppublish
Résumé
Light induces anthocyanin accumulation and hence decides the coloration of apple fruit. It also plays a key role in regulating the biosynthesis of other secondary metabolites. However, the crosstalk between anthocyanin and lignin metabolism during light induction, which affects the edible quality and visual quality of apple fruit, respectively, have rarely been characterized. In this study, we identified and functionally elucidated the roles of miR7125 and its target, cinnamoyl-coenzyme A reductase gene (CCR), in regulating the homeostasis between anthocyanin and lignin biosynthesis during light induction. Overexpressing miR7125 or inhibiting CCR transiently in apple fruit promoted anthocyanin biosynthesis but reduced lignin production under light-induced conditions. Consistently, opposite results were observed under the background of repressed miR7125 or overexpressed CCR. We found that the repressor MdMYB16 and the activator MdMYB1 bound to the miR7125 promoter. Transient repression of MdMYB16 upregulated miR7125 expression significantly, accompanied by decreased levels of MdCCR transcript, resulting in a reduction in the lignin biosynthesis and an increase in anthocyanin accumulation. However, transient overexpression of MdMYB16 produced the opposite effects to MdMYB16-RNAi. The results reveal a novel mechanism by which the MdMYB16/MdMYB1-miR7125-MdCCR module collaboratively regulates homeostasis between anthocyanin and lignin biosynthesis under light induction in apple.
Substances chimiques
Anthocyanins
0
Plant Proteins
0
Transcription Factors
0
Lignin
9005-53-2
Banques de données
GENBANK
['DQ341382']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1105-1122Informations de copyright
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
Références
Albert NW, Thrimawithana AH, McGhie TK, Clayton WA, Deroles SC, Schwinn KE, Bowman JL, Jordan BR, Davies KM. 2018. Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytologist 218: 554-566.
An JP, Liu YJ, Zhang XW, Bi SQ, Wang XF, You CX, Hao YJ. 2020. Dynamic regulation of different light intensity-modulated anthocyanin biosynthesis by BT2-TCP46-MYB1 in apple. Journal of Experimental Botany 71: 3094-3109.
Azuma A, Yakushiji H, Koshita Y, Kobayashi S. 2012. Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236: 1067-1080.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B: Statistical Methodology 57: 289-300.
Bruce RJ, West CA. 1989. Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiology 91: 889-897.
Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology 54: 519-546.
Chen W, Zhang M, Zhang G, Li P, Ma F. 2019. Differential regulation of anthocyanin synthesis in apple peel under different sunlight intensities. International Journal of Molecular Sciences 20: 1-13.
Daccord N, Celton J-M, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R et al. 2017. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genetics 49: 1099-1106.
Demura T, Fukuda H. 2007. Transcriptional regulation in wood formation. Trends in Plant Science 12: 64-70.
Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC. 2007. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. The Plant Journal 49: 414-427.
Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres J-L, Rovira P, Puigdomènech P et al. 2010. ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. The Plant Journal 64: 633-644.
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J. 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics 39: 1033-1037.
Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N. 2011. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Research 40: 37-52.
Ge H, Zhang J, Zhang YJ, Li X, Yin XR, Grierson D, Chen KS. 2017. EjNAC3 transcriptionally regulates chilling-induced lignification of loquat fruit via physical interaction with an atypical CAD-like gene. Journal of Experimental Botany 68: 5129-5136.
Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N et al. 2005. EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. The Plant Journal 43: 553-567.
Gonzalez A, Zhao M, Leavitt JM, Lloyd AM. 2008. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal 53: 814-827.
Hsu CC, Chen YY, Tsai WC, Chen WH, Chen HH. 2015. Three R2R3-MYB transcription factors regulate distinct floral pigmentation patterning in Phalaenopsis spp. Plant Physiology 168: 175-191.
Hu DG, Sun CH, Ma QJ, You CX, Cheng L, Hao YJ. 2016. MdMYB1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiology 170: 1315-1330.
Jin W, Wang H, Li M, Wang J, Yang Y, Zhang X, Yan G, Zhang H, Liu J, Zhang K. 2016. The R2R3 MYB transcription factor PavMYB10.1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L.). Plant Biotechnology Journal 14: 2120-2133.
Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T, Shimamoto K. 2006. Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proceedings of the National Academy of Sciences, USA 103: 230-235.
Khandal H, Singh AP, Chattopadhyay D. 2020. The MicroRNA397b-LACCASE2 module regulates root lignification under water- and phosphate deficiency. Plant Physiology 182: 1387-1403.
Lai B, Li XJ, Hu B, Qin YH, Huang XM, Wang HC, Hu GB. 2014. LcMYB1 is a key determinant of differential anthocyanin accumulation among genotypes, tissues, developmental phases and ABA and light stimuli in Litchi chinensis. PLoS ONE 9: e86293.
Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 103: R25.
Leplé J-C, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, Naumann A, Kang K-Y, Kim H, Ruel K et al. 2007. Downregulation of cinnamoyl-coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. The Plant Cell 19: 3669-3691.
Li P, Dong Q, Ge S, He X, Verdier J, Li D, Zhao J. 2016. Metabolic engineering of proanthocyanidin production by repressing the isoflavone pathways and redirecting anthocyanidin precursor flux in legume. Plant Biotechnology Journal 14: 1604-1618.
Li YY, Mao K, Zhao C, Zhao XY, Zhang HL, Shu HR, Hao YJ. 2012. MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiology 160: 1011-1022.
Lin JS, Lin CC, Lin HH, Chen YC, Jeng ST. 2012. MicroR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytologist 196: 427-440.
Mir Derikvand M, Sierra JB, Ruel K, Pollet B, Do CT, Thévenin J, Buffard D, Jouanin L, Lapierre C. 2008. Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227: 943-956.
Nguyen NH, Jeong CY, Kang GH, Yoo SD, Hong SW, Lee H. 2015. MYBD employed by HY5 increases anthocyanin accumulation via repression of MYBL2 in Arabidopsis. The Plant Journal 84: 1192-1205.
Ohlsson AB, Berglund T. 2001. Gibberellic acid-induced changes in glutathione metabolism and anthocyanin content in plant tissue. Plant Cell, Tissue and Organ Culture 64: 77-80.
Peng Z, Tian J, Luo R, Kang Y, Lu Y, Hu Y, Liu N, Zhang J, Cheng H, Niu S et al. 2019. MiR399d and epigenetic modification comodulate anthocyanin accumulation in Malus leaves suffering from phosphorus deficiency. Plant Cell and Environment 43: 1148-1159.
Péter G, Eberhard S, Ferenc N. 2003. Light perception and signalling in higher plants. Current Opinion in Plant Biology 6: 446-452.
Ring L, Yeh SY, Hücherig S, Hoffmann T, Blanco-Portales R, Fouche M, Villatoro C, Denoyes B, Monfort A, Caballero JL et al. 2013. Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiology 163: 43-60.
Scully ED, Gries T, Sarath G, Palmer NA, Baird L, Serapiglia MJ, Dien BS, Boateng AA, Ge Z, Funnell-Harris DL et al. 2016. Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. The Plant Journal 85: 378-395.
Shaipulah NF, Muhlemann JK, Woodworth BD, Van Moerkercke A, Verdonk JC, Ramirez AA, Haring MA, Dudareva N, Schuurink RC. 2016. CCoAOMT down-regulation activates anthocyanin biosynthesis in petunia. Plant Physiology 170: 717-731.
Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE, Jameson PE, Martin CR, Davies KM. 2011. The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytologist 189: 602-615.
Sharma D, Tiwari M, Pandey A, Bhatia C, Sharma A, Trivedi PK. 2016. MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant development. Plant Physiology 171: 944-959.
Shin DH, Choi M, Kim K, Bang G, Cho M, Choi SB, Choi G, Park YI. 2013. HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. Febs Letters 587: 1543-1547.
Su X, Zhao Y, Wang H, Li G, Cheng X, Jin Q, Cai Y. 2019. Transcriptomic analysis of early fruit development in Chinese white pear (Pyrus bretschneideri Rehd.) and functional identification of PbCCR1 in lignin biosynthesis. BMC Plant Biology 19: 417.
Sun Q, Liu X, Yang J, Liu W, Du Q, Wang H, Fu C, Li WX. 2018. MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Molecular Plant 11: 806-814.
Sun X, Wang C, Xiang N, Li X, Yang S, Du J, Yang Y, Yang Y. 2017. Activation of secondary cell wall biosynthesis by miR319-targeted TCP4 transcription factor. Plant Biotechnology Journal 15: 1284-1294.
Sun X, Zhang Z, Chen C, Wu W, Ren N, Jiang C, Yu J, Zhao Y, Zheng X, Yang Q et al. 2018. The C-S-A gene system regulates hull pigmentation and reveals evolution of anthocyanin biosynthesis pathway in rice. Journal of Experimental Botany 69: 1485-1498.
Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR. 2006. Light-induced expression of a MYB Gene regulates anthocyanin biosynthesis in red apples. Plant Physiology 142: 1216-1232.
Tian J, Peng Z, Zhang J, Song T, Wan H, Zhang M, Yao Y. 2015. McMYB10 regulates coloration via activating McF3′H and later structural genes in ever-red leaf crabapple. Plant Biotechnology Journal 13: 948-961.
Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28: 511-515.
Varet H, Brillet-Guéguen L, Coppée JY, Dillies MA. 2016. SARTools: A DESeq2- and EdgeR-Based R pipeline for comprehensive differential analysis of RNA-Seq data. PLoS ONE 11: e0157022.
Wang C-Y, Zhang S, Yu Y, Luo Y-C, Liu Q, Ju C, Zhang Y-C, Qu L-H, Lucas WJ, Wang X et al. 2014. MiR397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis. Plant Biotechnology Journal 12: 1132-1142.
Wang XF, An JP, Liu X, Su L, You CX, Hao YJ. 2018. The nitrate-responsive protein MdBT2 regulates anthocyanin biosynthesis by interacting with the MdMYB1 transcription factor. Plant Physiology 178: 890-906.
Wu HJ, Ma YK, Chen T, Wang M, Wang XJ. 2012. PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Research 40: W22-W28.
Xu H, Wang N, Liu J, Qu C, Wang Y, Jiang S, Lu N, Wang D, Zhang Z, Chen X. 2017. The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes. Plant Molecular Biology 94: 149-165.
Xu Q, Yin XR, Zeng JK, Ge H, Song M, Xu CJ, Li X, Ferguson IB, Chen KS. 2014. Activator- and repressor-type MYB transcription factors are involved in chilling injury induced flesh lignification in loquat via their interactions with the phenylpropanoid pathway. Journal of Experimental Botany 65: 4349-4359.
Xue C, Yao JL, Qin MF, Zhang MY, Allan AC, Wang DF, Wu J. 2019. PbrmiR397a regulates lignification during stone cell development in pear fruit. Plant Biotechnology Journal 17: 103-117.
Xue C, Yao JL, Xue YS, Su GQ, Wang L, Lin LK, Allan AC, Zhang SL, Wu J. 2019. PbrMYB169 positively regulates lignification of stone cells in pear fruit. Journal of Experimental Botany 70: 1801-1814.
Yang T, Ma H, Zhang J, Wu T, Song T, Tian J, Yao Y. 2019. Systematic identification of long noncoding RNAs expressed during light-induced anthocyanin accumulation in apple fruit. Plant Journal 100: 572-590.
Yousuf B, Gul K, Wani AA, Singh P. 2016. Health benefits of anthocyanins and their encapsulation for potential use in food systems: a review. Critical Reviews in Food Science and Nutrition 56: 2223-2230.
Yuan YW, Rebocho AB, Sagawa JM, Stanley LE, Bradshaw HD. 2016. Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species. Proceedings of the National Academy of Sciences, USA 113: 2448-2453.
Zhang J, Ge H, Zang C, Li X, Grierson D, Chen KS, Yin XR. 2016. EjODO1, a MYB transcription factor, regulating lignin biosynthesis in developing loquat (Eriobotrya japonica) fruit. Frontiers in Plant science 7: e76369.
Zhang Y, Xu S, Cheng Y, Peng Z, Han J. 2018. Transcriptome profiling of anthocyanin-related genes reveals effects of light intensity on anthocyanin biosynthesis in red leaf lettuce. PeerJ 6: e4607.
Zhao Y, Lin S, Qiu Z, Cao D, Wen J, Deng X, Wang X, Lin J, Li X. 2015. MicroRNA857 is involved in the regulation of secondary growth of vascular tissues in Arabidopsis. Plant Physiology 169: 2539-2552.
Zhong R, Ye ZH. 2009. Transcriptional regulation of lignin biosynthesis. Plant Signaling Behavior 4: 1028-1034.
Zhou L, Chen J, Li Z, Li X, Hu X, Huang Yi, Zhao X, Liang C, Wang Y, Sun L et al. 2010. Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS ONE 5: e15224.
Zhou LJ, Li YY, Zhang RF, Zhang CL, Xie XB, Zhao C, Hao Y-J. 2017. The small ubiquitin-like modifier E3 ligase MdSIZ1 promotes anthocyanin accumulation by sumoylating MdMYB1 under low-temperature conditions in apple. Plant, Cell & Environment 40: 2068-2080.
Zhu Z, Wang H, Wang Y, Guan S, Wang F, Tang J, Zhang R, Xie L, Lu Y. 2015. Characterization of the cis elements in the proximal promoter regions of the anthocyanin pathway genes reveals a common regulatory logic that governs pathway regulation. Journal of Experimental Botany 66: 3775-3789.