Plant Growth Regulation

, Volume 87, Issue 1, pp 9–18 | Cite as

Transcriptome profiles reveal new regulatory factors of anthocyanin accumulation in a novel purple-colored cherry tomato cultivar Jinling Moyu

  • Yinlei Wang
  • Zhidan Luo
  • Chen Lu
  • Rong Zhou
  • Huiming Zhang
  • Liping Zhao
  • Wengui Yu
  • TongMin ZhaoEmail author
Original paper


Anthocyanins are important secondary metabolites with high nutraceutical value. They represent the major red, purple, violet and blue pigments in higher plants but are usually not present in the fruits of domesticated tomatoes. Recently, several genes that regulate anthocyanin accumulation have been identified in wild tomatoes or mutation lines; however, whether there are other new factors involved in the regulation of anthocyanin biosynthesis is still unknown. “Jinling Moyu” (MY) is a novel purple cherry tomato that accumulates considerable anthocyanins in its ripe fruit. A transcriptome comparison analysis of MY fruits with pink and green fruit revealed that several structural genes assigned to the anthocyanin biosynthetic pathway were highly expressed in MY tomato, but all six known regulatory genes of anthocyanin accumulation in tomato fruits were rarely expressed among the samples in this study. However, four other R2R3–MYB and five other bHLH transcription factors were highly correlated with the differentially expressed structural genes in the anthocyanin pathway, indicating that these transcription factors might regulate anthocyanin biosynthesis in MY tomato. Our study will aid in understanding the complex mechanism regulating anthocyanin pigmentation in tomato fruits .


Tomato Purple fruit Anthocyanin Transcription factor 



We thank Drs. Jinhua Li and Yong Xue for their critical review of this manuscript. We also thank Springer-Nature Author Service for English Language Editing. This work was financially supported by the National Key Research and Development Plan [Grant No. 2016YFD0101703], the National Natural Science Foundation of China (Grant No. 31501763 and 31501022), Natural Science Foundation of Jiangsu Province, China (Grant No. BK20140440 and BK20140443) and the Jiangsu Agricultural Independent Innovation Foundation of China [Grant No. CX(14)5084].

Author contributions

YW designed the research, collected the samples and performed the anthocyanin extraction and quantification. ZL collected the samples, and performed the RNA isolation and qRT-PCR experiments. CL analyzed the RNA-Seq data and helped in manuscript writing. RZ and LZ helped in collecting the samples. HZ helped in data analysis. WY contributed to concept the idea. TZ designed the research and wrote the manuscript. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Supplementary material

10725_2018_444_MOESM1_ESM.pdf (320 kb)
Supplementary material 1 (PDF 319 KB)


  1. Abuqamar S, Luo H, Laluk K, Mickelbart MV, Mengiste T (2009) Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J 58(2):347–360CrossRefGoogle Scholar
  2. Albert NW et al (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26(3):962–980CrossRefGoogle Scholar
  3. Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13(3):99–102CrossRefGoogle Scholar
  4. Azuma K, Ohyama A, Ippoushi K, Ichiyanagi T, Takeuchi A, Saito T, Fukuoka H (2008) Structures and antioxidant activity of anthocyanins in many accessions of eggplant and its related species. J Agric Food Chem 56(21):10154–10159CrossRefGoogle Scholar
  5. Ballester AR et al (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152(1):71–84CrossRefGoogle Scholar
  6. Bassolino L, Zhang Y, Schoonbeek HJ, Kiferle C, Perata P, Martin C (2013) Accumulation of anthocyanins in tomato skin extends shelf life. New Phytol 200(3):650–655CrossRefGoogle Scholar
  7. Borghesi E et al (2016) Comparative physiology during ripening in tomato rich-anthocyanins fruits. Plant Growth Regul 80(2):207–214CrossRefGoogle Scholar
  8. Borovsky Y, Oren-Shamir M, Ovadia R, De Jong W, Paran I (2004) The A locus that controls anthocyanin accumulation in pepper encodes a MYB transcription factor homologous to Anthocyanin2 of Petunia. Theor Appl Genet 109(1):23–29CrossRefGoogle Scholar
  9. Bovy A, Schijlen E, Hall RD (2007) Metabolic engineering of flavonoids in tomato (Solanum lycopersicum): the potential for metabolomics. Metabolomics 3:399–412CrossRefGoogle Scholar
  10. Butelli E et al (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26(11):1301–1308CrossRefGoogle Scholar
  11. De Jong WS, Eannetta NT, De Jong DM, Bodis M (2004) Candidate gene analysis of anthocyanin pigmentation loci in the Solanaceae. Theor Appl Genet 108(3):423–432CrossRefGoogle Scholar
  12. Dhar MK, Sharma R, Koul A, Kaul S (2015) Development of fruit color in Solanaceae: a story of two biosynthetic pathways. Brief Funct Genomics 14(3):199–212CrossRefGoogle Scholar
  13. Goldsbrough A, Belzile F, Yoder JI (1994) Complementation of the tomato anthocyanin without (aw) mutant using the dihydroflavonol 4-reductase gene. Plant Physiol 105(2):491–496CrossRefGoogle Scholar
  14. Gonzali S, Mazzucato A, Perata P (2009) Purple as a tomato: towards high anthocyanin tomatoes. Trends Plant Sci 14(5):237–241CrossRefGoogle Scholar
  15. Gupta SK, Sharma S, Santisree P, Kilambi HV, Appenroth K, Sreelakshmi Y, Sharma R (2014) Complex and shifting interactions of phytochromes regulate fruit development in tomato. Plant Cell Environ 37(7):1688–1702CrossRefGoogle Scholar
  16. He J, Giusti MM (2010) Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 1:163–187CrossRefGoogle Scholar
  17. Hoffmann L et al (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16(6):1446–1465CrossRefGoogle Scholar
  18. Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7(7):1071–1083CrossRefGoogle Scholar
  19. Huang ZJ, Du YC, Qiu ZK, Cao X, Wang XY, Gao JC, Guo YM (2016) Molecular markers closely linked to tomato purple black fruit gene ATV and uses thereof. China Patent 201610405970.9Google Scholar
  20. Jones CM, Mes P, Myers JR (2003) Characterization and inheritance of the anthocyanin fruit (Aft) tomato. J Hered 94(6):449–456CrossRefGoogle Scholar
  21. Kang JH, McRoberts J, Shi F, Moreno JE, Jones AD, Howe GA (2014) The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiol 164(3):1161–1174CrossRefGoogle Scholar
  22. Khoo HE, Prasad KN, Kong KW, Jiang Y, Ismail A (2011) Carotenoids and their isomers: color pigments in fruits and vegetables. Molecules 16(2):1710–1738CrossRefGoogle Scholar
  23. Kiferle C et al (2015) Tomato R2R3-MYB proteins SlANT1 and SlAN2: same protein activity, different roles. PLoS ONE 10(8):e0136365CrossRefGoogle Scholar
  24. Li B, Ruotti V, Stewart RM, Thomson JA, Dewey CN (2010) RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26(4):493–500CrossRefGoogle Scholar
  25. Li H, Deng Z, Liu R, Loewen S, Tsao R (2014) Bioaccessibility, in vitro antioxidant activities and in vivo anti-inflammatory activities of a purple tomato (Solanum lycopersicum L.). Food Chem 159:353–360CrossRefGoogle Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25(4):402–408CrossRefGoogle Scholar
  27. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550CrossRefGoogle Scholar
  28. Maloney GS, DiNapoli KT, Muday GK (2014) The anthocyanin reduced tomato mutant demonstrates the role of flavonols in tomato lateral root and root hair development. Plant Physiol 166(2):614–631CrossRefGoogle Scholar
  29. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10–12CrossRefGoogle Scholar
  30. Mazzucato A et al (2013) Novel phenotypes related to the breeding of purple-fruited tomatoes and effect of peel extracts on human cancer cell proliferation. Plant Physiol Biochem 72:125–133CrossRefGoogle Scholar
  31. Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138(2):1083–1096CrossRefGoogle Scholar
  32. Mes PJ, Boches P, Myers JR, Durst R (2008) Characterization of tomatoes expressing anthocyanin in the fruit. J Am Soc Hortic Sci 133(2):262–269Google Scholar
  33. Morant M et al (2007) Catalytic activity, duplication and evolution of the CYP98 cytochrome P450 family in wheat. Plant Mol Biol 63(1):1–19CrossRefGoogle Scholar
  34. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14(4):417–419CrossRefGoogle Scholar
  35. Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181(3):219–229CrossRefGoogle Scholar
  36. Povero G, Gonzali S, Bassolino L, Mazzucato A, Perata P (2011) Transcriptional analysis in high-anthocyanin tomatoes reveals synergistic effect of Aft and atv genes. J Plant Physiol 168(3):270–279CrossRefGoogle Scholar
  37. Qiu Z, Wang X, Gao J, Guo Y, Huang Z, Du Y (2016) The tomato hoffman’s anthocyaninless gene encodes a bHLH transcription factor involved in anthocyanin biosynthesis that is developmentally regulated and induced by low temperatures. PLoS ONE 11(3):e0151067CrossRefGoogle Scholar
  38. Sapir M et al (2008) Molecular aspects of anthocyanin fruit tomato in relation to high pigment-1. J Hered 99(3):292–303CrossRefGoogle Scholar
  39. Schreiber G et al (2012) ANTHOCYANIN1 from Solanum chilense is more efficient in accumulating anthocyanin metabolites than its Solanum lycopersicum counterpart in association with the anthocyanin fruit phenotype of tomato. Theor Appl Genet 124(2):295–307CrossRefGoogle Scholar
  40. Schwinn K et al (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18(4):831–851CrossRefGoogle Scholar
  41. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140(2):637–646CrossRefGoogle Scholar
  42. Soneson C, Love MI, Robinson MD (2015) Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Res 4:1521CrossRefGoogle Scholar
  43. Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54(4):733–749CrossRefGoogle Scholar
  44. Torres CA, Davies NM, Yanez JA, Andrews PK (2005) Disposition of selected flavonoids in fruit tissues of various tomato (Lycopersicon esculentum mill.) Genotypes. J Agric Food Chem 53(24):9536–9543CrossRefGoogle Scholar
  45. Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493CrossRefGoogle Scholar
  46. Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5):284–287CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institute of Vegetable CropsJiangsu Academy of Agricultural SciencesNanjingChina
  2. 2.Jiangsu Key Laboratory for Horticultural Crop Genetic ImprovementNanjingChina
  3. 3.Lianyungang Institute of Agricultural Sciences in Jiangsu Xuhuai AreaJiangsu Academy of Agricultural SciencesLianyungangChina
  4. 4.Jiangsu Key Laboratory of Marine Pharmaceutical Compound ScreeningHuaihai Institute of TechnologyLianyungangChina
  5. 5.Co-Innovation Center of Jiangsu Marine Bio-industry TechnologyHuaihai Institute of TechnologyLianyungangChina
  6. 6.Jiangsu Marine Resources Development Research InstituteLianyungangChina
  7. 7.Jiangsu Yugong Biolabs Inc.LianyungangChina

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