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Arabidopsis AtPAP1 transcription factor induces anthocyanin production in transgenic Taraxacum brevicorniculatum

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Abstract

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This study developed a new purple coloured Taraxacum brevicorniculatum plant through genetic transformation using the Arabidopsis AtPAP1 gene, which overproduced anthocyanins in its vegetative tissues.

Abstract

Rubber-producing Taraxacum plants synthesise high-quality natural rubber (NR) in their roots and so are a promising alternative global source of this raw material. A major factor in its commercialization is the need for multipurpose exploitation of the whole plant. To add value to the aerial tissues, red/purple plants of the rubber-producing Taraxacum brevicorniculatum species were developed through heterologous expression of the production of anthocyanin pigment 1 (AtPAP1) transcription factor from Arabidopsis thaliana. The vegetative tissue of the transgenic plants showed an average of a 48-fold increase in total anthocyanin content over control levels, but with the exception of pigmentation, the transgenic plants were phenotypically comparable to controls and displayed similar growth vigor. Southern blot analysis confirmed that the AtPAP1 gene had been integrated into the genome of the high anthocyanin Taraxacum plants. The AtPAP1 expression levels were estimated by quantitative real-time PCR and were highly correlated with the levels of total anthocyanins in five independent transgenic lines. High levels of three cyanidin glycosides found in the purple plants were characterized by high performance liquid chromatography–mass spectrum analysis. The presence of NR was verified by NMR and infrared spectroscopy, and confirmed that NR biosynthesis had not been affected in the transgenic Taraxacum lines. In addition, other major phenylpropanoid products such as chlorogenic acid and quercetin glycosides were also enhanced in the transgenic Taraxacum. The red/purple transgenic Taraxacum lines described in this study would increase the future application of the species as a rubber-producing crop due to its additional health benefits.

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Abbreviations

MS:

Murashige and Skoog medium

HPLC:

High performance liquid chromatography

HPLC–MS:

High performance liquid chromatography–mass spectrum

NMR:

Nuclear magnetic resonance

GUS:

β-Glucuronidasegene

CPT:

Cis-prenyltransferase

SRPP:

Small rubber particle protein

PAL:

Phenylalanine ammonia lyase

C4H:

Cinnamate 4-monooxygenase

C3H:

Coumarate 3-hydroxylase

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

F3H:

Flavanone 3-hydroxylase

CaMV 35S:

Cauliflower mosaic virus 35S promoter

References

  • Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int J Mol Sci 14:3540–3555

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52(1):98–111

    Article  PubMed  CAS  Google Scholar 

  • Buranov AU, Elmuradov BJ (2010) Extraction and characterization of latex and natural rubber from rubber-bearing plants. J Agric Food Chem 58:734–743

    Article  PubMed  CAS  Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EG, Hall RD, Bovy AG, Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb Protoc. doi:10.1101/pdb.prot5177

    Google Scholar 

  • Collins-Silva J, Nural AT, Skaggs A, Scott D, Hathwaik U, Woolsey R, Schegg K, McMahan C, Whalen M, Cornish K, Shintani D (2012) Altered levels of the Taraxacum kok-saghyz (Russian dandelion) small rubber particle protein, TkSRPP3, result in qualitative and quantitative changes in rubber metabolism. Phytochemistry 79:46–56

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA, Liu C, Jun JH (2013) Metabolic engineering of anthocyanins and condensed tannins in plants. Curr Opin Biotechnol 24:329–335

    Article  PubMed  CAS  Google Scholar 

  • Elomaa P, Uimari A, Mehto M, Albert VA, Laitinen RA, Teeri TH (2003) Activation of anthocyanin biosynthesis in Gerbera hybrida (Asteraceae) suggests conserved protein–protein and protein-promoter interactions between the anciently diverged monocots and eudicots. Plant Physiol 133:1831–1842

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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. Plant J 49:414–427

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116

    Article  PubMed  CAS  Google Scholar 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780

    Article  PubMed  CAS  Google Scholar 

  • Hillebrand A, Post JJ, Wurbs D, Wahler D, Lenders M, Krzyzanek V, Prufer D, Gronover CS (2012) Down-regulation of small rubber particle protein expression affects integrity of rubber particles and rubber content in Taraxacum Brevicorniculatum. PLoS One. doi:10.1371/journal.pone.0041874

    Google Scholar 

  • Kirschner J, Štěpánek J, Černý T, Peter DH, Peter J, Dijk van (2013) Available exsitu germplasm of the potential rubber crop Taraxacum Koksaghyz belongs to a poor rubber producer, T. Brevicorniculatum (Compositae–Crepidinae). Genet Resour Crop Ev 60:455–471

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242

    Article  PubMed  CAS  Google Scholar 

  • Krotkov G (1945) A review of literature on Taraxacum kok-saghyz. Rod Bot Rev 11:417–461

    Article  CAS  Google Scholar 

  • Kuhn BM, Geisler M, Bigler L, Ringli C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 156:585–595

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Laitinen RA, Ainasoja M, Broholm SK, Teeri TH, Elomaa P (2008) Identification of target genes for a MYB-type anthocyanin regulator in Gerbera hybrida. J Exp Bot 59:3691–3703

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430

    Article  PubMed  CAS  Google Scholar 

  • Li H, Flachowsky H, Fischer TC, Hanke MV, Forkmann G, Treutter D, Schwab W, Hoffmann TS, Zankowski I (2007) Maize Lc Transcription Factor enhances biosynthesis of anthocyanins, distinct proanthocyanidins and phenylpropanoids in apple (Malus Domestica Borkh.). Planta 226:1243–1254

    Article  PubMed  CAS  Google Scholar 

  • Li X, Gao MJ, Pan HY, Cui DJ, Gruber MY (2010) Purple canola: Arabidopsis PAP1 increases antioxidants and phenolics in Brassica napus leaves. J Agric Food Chem 58:1639–1645

    Article  PubMed  CAS  Google Scholar 

  • Li X, Ma H, Huang H, Li D, Yao S (2013) Natural anthocyanins from phytoresources and their chemical researches. Nat Prod Res 27:456–469

    Article  PubMed  CAS  Google Scholar 

  • Munt O, Arias M, Hernandez M, Ritter E, Gronover CS, Prüfera D (2012) Fertilizer and planting strategies to increase biomass and improve root morphology in the natural rubber producer taraxacum brevicorniculatum. Ind Crops Prod 36:289–293

    Article  CAS  Google Scholar 

  • Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6:3553–3558

    PubMed Central  PubMed  CAS  Google Scholar 

  • Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181:219–229

    Article  PubMed  CAS  Google Scholar 

  • Post J, van Deenen N, Fricke J, Kowalski N, Wurbs D, Schaller H, Eisenreich W, Huber C, Twyman RM, Prufer D, Gronover CS (2012) Laticifer-specific cis-prenyltransferase silencing affects the rubber, triterpene, and inulin content of Taraxacum Brevicorniculatum. Plant Physiol 158:1406–1417

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Qiu J, Gao F, Shen G, Li C, Han X, Zhao Q, Zhao D, Hua X, Pang Y (2013) Metabolic engineering of the phenylpropanoid pathway enhances the antioxidant capacity of Saussurea involucrata. PLoS One. doi:10.1371/journal.pone.0070665

    Google Scholar 

  • Quattrocchio FM (1994) Regulatory genes controlling flower pigmentation in petunia hybrida. PhD thesis, Vrije University, Netherlands

  • Rowan DD, Cao M, Lin-Wang K, Cooney JM, Jensen DJ, Austin PT, Hunt MB, Norling C, Hellens RP, Schaffer RJ, Allan AC (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182:102–115

    Article  PubMed  CAS  Google Scholar 

  • Schmidt T, Lenders M, Hillebrand A, van Deenen N, Munt O, Reichelt R, Eisenreich W, Fischer R, Prufer D, Gronover CS (2010) Characterization of rubber particles and rubber chain elongation in Taraxacum koksaghyz. BMC Biochem. doi:10.1186/1471-2091-11-11

    PubMed Central  PubMed  Google Scholar 

  • Schutz K, Carle R, Schieber A (2006) Taraxacum—a review on its phytochemical and pharmacological profile. J Ethnopharmacol 107:313–323

    Article  PubMed  CAS  Google Scholar 

  • Suchat S, Pioch D, Palu S, Tardan E, Loo ENv, Davrieux F (2013) Fast determination of the resin and rubber content in Parthenium argentatum biomass using near infrared spectroscopy. Ind Crops Prod 45:44–51

    Article  CAS  Google Scholar 

  • van Beilen JB, Poirier Y (2007a) Establishment of new crops for the production of natural rubber. Trends Biotechnol 25:522–529

    Article  PubMed  CAS  Google Scholar 

  • van Beilen JB, Poirier Y (2007b) Guayule and Russian dandelion as alternative sources of natural rubber. Crit Rev Biotechnol 27:217–231

    Article  PubMed  CAS  Google Scholar 

  • Wahler D, Gronover CS, Richter C, Foucu F, Twyman RM, Moerschbacher BM, Fischer R, Muth J, Prufer D (2009) Polyphenoloxidase silencing affects latex coagulation in Taraxacum Species. Plant Physiol 151:334–346

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Whaley WG, Bowen JS (1947) Russian Dandelion (kok-saghyz). An emergency source of natural rubber. USDA Miscellaneous Publication 618, Washington, DC

  • Zhao J, Li ZT, Chen J, Henny RJ, Gray DJ, Chen J (2013) Purple-leaved Ficus lyrata plants produced by overexpressing a grapevine VvMybA1 gene. Plant Cell Rep 32:1783–1793

    Article  PubMed  CAS  Google Scholar 

  • Zhou LL, Zeng HN, Shi MZ, Xie DY (2008) Development of tobacco callus cultures over expressing Arabidopsis PAP1/MYB75 transcription factor and characterization of anthocyanin biosynthesis. Planta 229:37–51

    Article  PubMed  CAS  Google Scholar 

  • Zuluaga DL, Gonzali S, Loreti E, Pucciariello C, Degl’Innocenti ED, Guidi L, Alpi A, Perata P (2008) Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. Funct Plant Biol 35:606–618

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-34) and the Shandong Linglong Tyre Company Limited.

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Authors and Affiliations

  1. The Key Laboratory of Biology and Genetic Resources of Rubber Tree, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, 571737, Hainan, China

    Jian Qiu, Shiqiao Luo, Xianzhou Xiao & Shizhong Liu

  2. Zhanjiang Experiment Station, Chinese Academy of Tropical Agricultural Sciences, Zhanjiang, 524013, Guangdong, China

    Shizhong Liu

  3. Center of Advanced Elastomer Materials, College of Materials and Engineering, Beijing University of Chemical and Technology, Beijing, 100029, China

    Shuquan Sun, Jichuan Zhang & Liqun Zhang

  4. Shandong Linglong Tyre Company Limited, Zhaoyuan, 265406, Shandong, China

    Feng Wang

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  1. Jian Qiu
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  2. Shuquan Sun
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  3. Shiqiao Luo
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  4. Jichuan Zhang
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  5. Xianzhou Xiao
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  6. Liqun Zhang
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  7. Feng Wang
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  8. Shizhong Liu
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Corresponding author

Correspondence to Shizhong Liu.

Additional information

Communicated by A. Dhingra.

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Qiu, J., Sun, S., Luo, S. et al. Arabidopsis AtPAP1 transcription factor induces anthocyanin production in transgenic Taraxacum brevicorniculatum . Plant Cell Rep 33, 669–680 (2014). https://doi.org/10.1007/s00299-014-1585-8

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  • DOI: https://doi.org/10.1007/s00299-014-1585-8

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