Skip to main content
Log in

Differential expression of anthocyanin structural genes and transcription factors determines coloration patterns in gerbera flowers

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

We investigated the expression of anthocyanin structural genes and transcription factors (TFs) associated with varying anthocyanin content during different developmental stages (S1–S4) of the gerbera cultivars ‘Nathasha’ and ‘Rosalin’. Accumulation of anthocyanin started at S1 and reached a maximum at S3 in both cultivars. Enhancement of anthocyanin content in ‘Nathasha’ was associated with upregulation of ANS and MYB10, whereas in ‘Rosalin’, upregulation was associated with CHS1, MYB10, and MYC1. Low-temperature exposure (6 °C) enhanced anthocyanin content to a greater extent than that at 22 °C via stronger upregulation of CHS1 and MYB10 in ‘Nathasha’ and CHS1 in ‘Rosalin’, irrespective of flower developmental stage. However, differences in anthocyanin content between the two cultivars were found to be influenced by the expression levels of all structural genes and TFs, irrespective of flower developmental stage and temperature conditions. We suggest that differences in the regulation mechanisms of anthocyanin biosynthesis and coloration pattern between ‘Nathasha’ and ‘Rosalin’ are related to differences in the expression patterns of structural genes and TFs; however, further functional studies of the key genes in anthocyanin biosynthesis are needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

PAL :

Phenylalanine ammonia lyase

CHS :

Chalcone synthase

F3H :

Flavanone-3-hydroxylase

F3′H :

Flavonoid 3′ hydroxylase

ANS :

Anthocyanidin synthase

DFR :

Dihydroflavonol-4-reductase

UFGT :

UDP-glycose flavonoid 3-O-glycosyl transferase

bHLH:

Basic helix–loop–helix

TF:

Transcription factor

References

  • Ai TN, Naing AH, Arun M, Kim CK (2016) Sucrose-induced anthocyanin accumulation in vegetative tissue of Petunia plants requires anthocyanin regulatory transcription factor genes. Plant Sci 252:144–150

    Article  CAS  PubMed  Google Scholar 

  • Ban Y, Honda C, Hatsuyama Y, Igarashi M, Hideo Bessho H, Moriguchi T (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red colouration in apple skin. Plant Cell Physiol 48:958–970

    Article  CAS  PubMed  Google Scholar 

  • Bashandy H, Pietiäinen M, Carvalho E, Lim K-J, Elomaa P, Martens S, Teeri TH (2015) Anthocyanin biosynthesis in gerbera cultivar ‘Estelle’ and its acyanic sport ‘Ivory’. Planta 242:601–611

    Article  CAS  PubMed  Google Scholar 

  • Biran I, Halevy AH (1973) Effect of short-term heat and shade treatments on petal colour of ‘baccara’ roses. Physiol Plant 31:180–185

    Article  Google Scholar 

  • Biran I, Enoch H, Zieslinand N, Helevy A (1973) The influence of light intensity, temperature and carbon dioxide concentration on anthocyanin content and bluing of ‘baccara’ roses. Sci Hortic 1:157–164

    Article  Google Scholar 

  • Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Opin Plant Biol 8:272–279

    Article  CAS  PubMed  Google Scholar 

  • Chandler S, Tanaka Y (2007) Genetic modification in floriculture. Crit Rev Plant Sci 26:169–197

    Article  CAS  Google Scholar 

  • Collette VE, Jameson PE, Schwinn KE, Umaharan P, Davies KM (2004) Temporal and spatial expression of flavonoid biosynthetic genes in flowers of Anthurium andraeanum. Physiol Plant 122:297–304

    Article  CAS  Google Scholar 

  • Dela G, Or E, Ovadia A, Nissim-Levi A, Weiss D, Oren-Shamir M (2003) Changes in anthocyanin concentration and composition in ‘jaguar’ rose flowers due to transient high-temperature conditions. Plant Sci 164:333–340

    Article  CAS  Google Scholar 

  • Deng X, Bashandy H, Ainasoja M, Kontturi J, Pietiäinen M, Laitinen R, Albert VA, Valkonen JP, Elomaa P, Teeri TH (2014) Functional diversification of duplicated chalcone synthase genes in anthocyanin biosynthesis of Gerbera hybrida. New Phytol 201:1469–1483

    Article  CAS  PubMed  Google Scholar 

  • Elomaa P, Mehto M, Kotilainen M, Helariutta Y, Nevalainen L, Teeri TH (1998) A bHLH transcription factor mediates organ, region and flower type specific signals on dihydroflavonol- 4-reductase (dfr) gene expression in the inflorescence of Gerbera hybrida (Asteraceae). Plant J 16:93–99

    Article  CAS  PubMed  Google Scholar 

  • Elomaa P, Uimari A, Mehto M, Albert VA, Laitinen RAE, 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guo N, Cheng F, Wu J, Liu B, Zheng SN, Liang JL, Wang XW (2014) Anthocyanin biosynthetic genes in Brassica rapa. BMC Genom 15:426

    Article  CAS  Google Scholar 

  • Hansen HV (1999) A story of the cultivated Gerbera. New Plantsman 6:85–95

    Google Scholar 

  • Helariutta Y, Elomaa P, Kotilainen M, Seppeanen P, Teeri TH (1993) Cloning of cDNA coding for dihydroflavonol-4-reductase (DFR) and characterization of dfr expression in the corollas of Gerbera hybrida var Regina (Compositae). Plant Mol Biol. 22:183–93

  • Helariutta Y, Elomaa P, Kotilainen M, Griesbach RJ, Schreoder J, Teeri TH (1995) Chalcone synthase-like genes active during corolla development are differentially expressed and encode enzymes with different catalytic properties in Gerbera hybrida (Asteraceae). Plant Mol Biol 28:47–60

    Article  CAS  PubMed  Google Scholar 

  • Helariutta Y, Kotilainen M, Elomaa P, Kalkkinen N, Bremer K, Teeri TH, Albert V (1996) Duplication and functional divergence in the chalcone synthase gene family of Asteraceae: evolution with substrate change and catalytic simplification. Proc Nat Acad Sci USA 93:9033–9038

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Lai YS, Yamagishi M, Suzuki T (2011) Elevated temperature inhibits anthocyanin biosynthesis in the tepals of an Oriental hybrid lily via the suppression of LhMYB12 transcription. Sci Hortic 132:59–65

    Article  CAS  Google Scholar 

  • Laitinen RAE, Immanen J, Auvinen P, Rudd S, Alatalo E, Paulin L, Ainasoja M, Kotilainen M, Koskela S, Teeri TH (2005) Analysis of the floral transcriptome uncovers new regulators of organ determination and gene families related to flower organ differentiation in Gerbera hybrida (Asteraceae). Genom Res 15:475–486

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyva A, Jarillo JA, Salinas J, Martinez-Zapater JM (1995) Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol 108:39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin-Wang K, Micheletti D, Palmer J (2011) High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Env 34:1176–1190

    Article  CAS  Google Scholar 

  • Lo Piero AR, Puglisi I, Rapisarda P, Petrone G (2005) Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. J Agric Food Chem 53:9083–9088

    Article  CAS  PubMed  Google Scholar 

  • Martens S, Teeri T, Forkmann G (2002) Heterologous expression of dihydroflavonol 4-reductases from various plants. FEBS Lett 531:453–458

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Gerats T (1993) The control of pigment biosynthesis genes during petal development. Plant Cell 5:1253–1264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng XC, Xing T, Wang X (2004) The role of light in the regulation of anthocyanin accumulation in Gerbera hybrid. Plant Growth Reg 44:243–250

    Article  CAS  Google Scholar 

  • Nakatsuka T, Nishihara M, Mishiba K, Yamamura S (2005) Temporal expression of flavonoid biosynthesis related genes regulates flower pigmentation in gentian plants. Plant Sci 168:1309–1318

    Article  CAS  Google Scholar 

  • Nozaki K, Takamura T, Fukai S (2006) Effects of high temperature on flower colour and anthocyanin content in pink flower genotypes of greenhouse chrysanthemum (Chrysanthemum morifolium Ramat.). J Hortic Sci Biotechnol 81:728–734

    Article  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  CAS  PubMed  Google Scholar 

  • Plasmeijer J, Yanai Y (2012) Floriculture Products Report 2012. Issue No. M12 (2011), 9 January 2012. Market News Service of International Trade Center

  • Quattrocchio F, Wing JF, van der Woude K, Mol JNM, Koes R (1998) Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J 13:475–488

    Article  CAS  PubMed  Google Scholar 

  • Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006) PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell 18:1274–1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosati C, Cadic A, Duron M, Ingouff M, Simoneaub P (1999) Molecular characterization of the anthocyanidin synthase gene in Forsythia × intermedia reveals organ-specific expression during flower development. Plant Sci 149:73–79

    Article  CAS  Google Scholar 

  • Rowan DD, Cao M, Lin-Wang K (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182:102–115

    Article  CAS  PubMed  Google Scholar 

  • Schwinn KE, Davies KM (2004) Flavonoids. In: Davies K (ed) Plant pigments and their manipulation. Blackwell Publishing Ltd, Oxford, pp 92–149

    Google Scholar 

  • Seitz C, Eder C, Deiml B, Kellner S, Martens S, Forkmann G (2006) Cloning, functional identification and sequence analysis of flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase cDNAs reveals independent evolution of flavonoid 3′,5′-hydroxylase in the Asteraceae family. Plant Mol Biol 61:365–381

    Article  CAS  PubMed  Google Scholar 

  • Shimizu K, Ohnishi N, Morikawa N, Ishigami A, Otake S, Rabah IO (2011) A 94-bp deletion of anthocyanidin synthase gene in acyanic flower lines of lisianthus [Eustoma grandiflorum. (Raf.) Shinn]. J Jpn Soc Hortic Sci 80:434–442

    Article  CAS  Google Scholar 

  • Shvarts M, Borochov A, Weiss D (1997) Low temperature enhances petunia flower pigmentation and induces chalcone synthase gene expression. Physiol Plant 99:67–72

    Article  CAS  Google Scholar 

  • Takos AM, Jaffe´ FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Biotech J 13:948–961

    Article  CAS  Google Scholar 

  • Wang Y, Shi S, Zhou Y, Zhou Y, Yang J, Tang X (2016) Genomewide identification and characterization of GRAS transcription factors in sacred lotus (Nelumbo nucifera). Peer J 4:e2388

    Article  CAS  PubMed  Google Scholar 

  • Wellmann F, Griesser M, Schwab W, Martens S, Eisenreich W, Matern U, Lukacin R (2006) Anthocyanidin synthase from Gerbera hybrida catalyzes the conversion of (+)-catechin to cyanidin and a novel procyanidin. FEBS Letts 580:1642–1648

    Article  CAS  Google Scholar 

  • Wessinger CA, Rausher MD (2014) Predictability and irreversibility of genetic changes associated with flower color evolution in Penstemon barbatus. Evolution 68:1058–1070

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi M, Shimoyamada Y, Nakatsuka T, Masuda K (2010) Two R2R3-MYB genes, homologs of Petunia AN2, regulate anthocyanin biosyntheses in flower tepals, tepal spots and leaves of asiatic hybrid lily. Plant Cell Physiol 51:463–474

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Butelli E, Martin C (2014) Engineering anthocyanin biosynthesis in plants. Curr Opin Plant Biol 19:81–90

    Article  CAS  PubMed  Google Scholar 

  • Zhao DQ, Tao J, Han CX, Ge JT (2012) Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.). Mol Biol Rep 39:11263–11275

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET), through the Agri-Bio Industry Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA) (Grant #: 315002-5). The funding body did not play a role in the design of the study and writing of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

AHN designed the study, conducted the experiments, and wrote the manuscript. CKK supervised experiments at all stages and performed critical revisions of the manuscript. DYP and KIP were involved in qRT-PCR analysis and interpretation of the data. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Chang Kil Kim.

Ethics declarations

Conflict of interest

There is no conflict of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naing, A.H., Park, D.Y., Park, K.I. et al. Differential expression of anthocyanin structural genes and transcription factors determines coloration patterns in gerbera flowers. 3 Biotech 8, 393 (2018). https://doi.org/10.1007/s13205-018-1408-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-018-1408-7

Keywords

Navigation