Skip to main content
Log in

Comparative gene expression analysis in a highly anthocyanin pigmented mutant of colorless chrysanthemum

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

In this study, we investigated differentially expressed genes between the original chrysanthemum cultivar ‘Argus’ with white flower color and its gamma-ray irradiated mutant ‘ARTI-purple’ with purple flower color. The expression levels of anthocyanin biosynthetic genes were not associated with anthocyanin accumulations of Argus and ARTI-purple. Expressed sequence tags (ESTs) analysis was performed to identify a novel cDNAs encoding enzymes of specific plant metabolic pathways and the biological effects of gamma-ray mutation through alterations in expression in each flower. A total of 796 unigenes were isolated from chrysanthemum ray florets. These unigenes were functionally classified using gene ontologies and tentative pathway associations were established to 99 sequences in the Kyoto encyclopedia of genes and genomes. The expressions of the isolated ESTs were screened by cDNA dot blot hybridization. Seven differentially expressed genes were identified as being involved in carbohydrate and lipid metabolic pathways and five as transcription factor or signal transduction genes. Of particular note, decreased expression of CmMYB1 was identified at the ‘ARTI-purple’. The CmMYB1 shared high similarity with AtMYB4 and AtMYBL2 which is a negative regulator of anthocyanin and flavonol accumulation. Furthermore, two genes involved in lipid metabolism, enoyl-ACP reductase and [acyl-carrier-protein] S-malonyltransferase, were decreased in the ‘ARTI-purple’ flower. Our results suggest that the purple pigmentation of the ‘ARTI-purple’ is not just dependent on the expression of anthocyanin synthesis genes, and that the pigmentation may also affect other metabolic processing and the plant cell environment.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Goodhead DT (1994) Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol 65(1):7–17

    Article  PubMed  CAS  Google Scholar 

  2. H.J.M B (1961) Radiosensitivity of higher plants, and correlations with cell weight and DNA content. Radiat Bot 1:223–228

    Article  Google Scholar 

  3. Uauy C, Paraiso F, Colasuonno P, Tran R, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified tilling approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9(1):115

    Article  PubMed  Google Scholar 

  4. Prithivirajsingh S, Story MD, Bergh SA, Geara FB, Ang KK, Ismail SM, Stevens CW, Buchholz TA, Brock WA (2004) Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett 571(1–3):227–232

    Article  PubMed  CAS  Google Scholar 

  5. Yamaguchi H, Shimizu A, Degi K, Morishita T (2008) Effects of dose and dose rate of gamma ray irradiation on mutation induction and nuclear DNA content in chrysanthemum. Breed Sci 58(3):331–335

    Article  Google Scholar 

  6. Wi SG, Chung BY, Kim J-S, Kim J-H, Baek M-H, Lee J-W, Kim YS (2007) Effects of gamma irradiation on morphological changes and biological responses in plants. Micron 38(6):553–564

    Article  PubMed  CAS  Google Scholar 

  7. Nagata T, Todoriki S, Hayashi T, Shibata Y, Mori M, Kanegae H, Kikuchi S (1999) r-Radiation induces leaf trichome formation in Arabidopsis. Plant Physiol 120(1):113–120

    Article  PubMed  CAS  Google Scholar 

  8. Kim DS, Kim J-B, Goh EJ, Kim W-J, Kim SH, Seo YW, Jang CS, Kang S-Y (2011) Antioxidant response of Arabidopsis plants to gamma irradiation: genome-wide expression profiling of the ROS scavenging and signal transduction pathways. J Plant Physiol 168(16):1960–1971

    Article  PubMed  CAS  Google Scholar 

  9. Ayed N, Yu HL, Lacroix M (1999) Improvement of anthocyanin yield and shelf-life extension of grape pomace by gamma irradiation. Food Res Int 32(8):539–543

    Article  CAS  Google Scholar 

  10. Alothman M, Bhat R, Karim AA (2009) Effects of radiation processing on phytochemicals and antioxidants in plant produce. Trends Food Sci Technol 20(5):201–212

    Article  CAS  Google Scholar 

  11. Boss PK, Davies C, Robinson SP (1996) Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv shiraz grape berries and the implications for pathway regulation. Plant Physiol 111(4):1059–1066

    PubMed  CAS  Google Scholar 

  12. Iida S, Hoshino A, Johzuka-Hisatomi Y, Habu Y, Inagaki Y (1999) Floricultural traits and transposable elements in the Japanese and common morning gloriesaa. Ann N Y Acad Sci 870(1):265–274

    Article  PubMed  CAS  Google Scholar 

  13. Yamaguchi TKusumi, Nishino T (2001) Malonyl-CoA: anthocyanin 5-O-glucoside-6′″-O-malonyltransferase from scarlet sage (Salvia splendens) flowers. J Biol Chem 276(52):49013–49019

    Article  PubMed  Google Scholar 

  14. Oren-Shamir M (2009) Does anthocyanin degradation play a significant role in determining pigment concentration in plants? Plant Sci 177(4):310–316

    Article  CAS  Google Scholar 

  15. Asen S, Stewart RN, Norris KH (1975) Anthocyanin, flavonol copigments, and pH responsible for larkspur flower color. Phytochemistry 14(12):2677–2682

    Article  CAS  Google Scholar 

  16. Shaked-Sachray L, Weiss D, Reuveni M, Nissim-Levi A, Oren-Shamir M (2002) Increased anthocyanin accumulation in aster flowers at elevated temperatures due to magnesium treatment. Physiol Plant 114(4):559–565

    Article  PubMed  CAS  Google Scholar 

  17. Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179(4):1004–1016

    Article  PubMed  CAS  Google Scholar 

  18. Jeong ST, Goto-Yamamoto N, Kobayashi S, Esaka M (2004) Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci 167(2):247–252

    Article  CAS  Google Scholar 

  19. Aharoni A, De Vos CHR, Wein M, Sun Z, Greco R, Kroon A, Mol JNM, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28(3):319–332

    Article  PubMed  CAS  Google Scholar 

  20. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19(22):6150–6161

    Article  PubMed  CAS  Google Scholar 

  21. Matsui K, Umemura Y, Ohme-Takagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55(6):954–967

    Article  PubMed  CAS  Google Scholar 

  22. Ohlrogge J, Benning C (2000) Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol 3(3):224–228

    CAS  Google Scholar 

  23. Chen S, Miao H, Chen F, Jiang B, Lu J, Fang W (2009) Analysis of expressed sequence tags (ESTs) collected from the inflorescence of chrysanthemum. Plant Mol Biol Rep 27(4):503–510

    Article  CAS  Google Scholar 

  24. Jurd L, Asen S (1966) The formation of metal and “co-pigment” complexes of cyanidin 3-glucoside. Phytochemistry 5(6):1263–1271

    Article  CAS  Google Scholar 

  25. Harada T, Torii Y, Morita S, Masumura T, Satoh S (2010) Differential expression of genes identified by suppression subtractive hybridization in petals of opening carnation flowers. J Exp Bot 61(9):2345–2354

    Article  PubMed  CAS  Google Scholar 

  26. Durbin ML, McCaig B, Clegg MT (2000) Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol Biol 42(1):79–92

    Article  PubMed  CAS  Google Scholar 

  27. Harker CL, Ellis T, Coen ES (1990) Identification and genetic regulation of the chalcone synthase multigene family in pea. Plant Cell 2(3):185–194

    PubMed  CAS  Google Scholar 

  28. Berardini T, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller L, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee S (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:745–755

    Article  PubMed  CAS  Google Scholar 

  29. Courtney-Gutterson N, Firoozabady E, Lemieux C, Nicholas J, Morgan A, Robinson K, Otten A, Akerboom M (1993) Production of genetically engineered color-modified chrysanthemum plants carrying a homologous chalcone synthase gene and their field performance. Acta Hortic 336:57–62

    Google Scholar 

  30. 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):637–646

    Article  PubMed  CAS  Google Scholar 

  31. Kobayashi S, Ishimaru M, Ding CK, Yakushiji H, Goto N (2001) Comparison of udp-glucose:flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci 160(3):543–550

    Article  PubMed  CAS  Google Scholar 

  32. Kovinich N, Saleem A, Arnason JT, Miki B (2010) Functional characterization of a UDP-glucose:flavonoid 3-O-glucosyltransferase from the seed coat of black soybean (Glycine max (L.) merr.). Phytochemistry 71(11–12):1253–1263

    Article  PubMed  CAS  Google Scholar 

  33. Suzuki H, Nakayama T, Yonekura-Sakakibara K, Fukui Y, Nakamura N, Nakao M, Tanaka Y, Tohge M-A, Nishiyama TY, Hirai MY, Yano M, Nakajima J-I, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42(2):218–235

    Article  Google Scholar 

  34. Ogata J, Kanno Y, Itoh Y, Tsugawa H, Suzuki M (2005) Plant biochemistry: anthocyanin biosynthesis in roses. Nature 435(7043):757–758

    Article  PubMed  CAS  Google Scholar 

  35. Unno H, Ichimaida F, Suzuki H, Takahashi S, Tanaka Y, Saito A, Nishino T, Kusunoki M, Nakayama T (2007) Structural and mutational studies of anthocyanin malonyltransferases establish the features of BAHD enzyme catalysis. J Biol Chem 282(21):15812–15822

    Article  PubMed  CAS  Google Scholar 

  36. Suzuki H, Nakayama T, Yamaguchi M-A, Nishino T (2004) cDNA cloning and characterization of two Dendranthema  × morifolium anthocyanin malonyltransferases with different functional activities. Plant Sci 166(1):89–96

    Article  CAS  Google Scholar 

  37. Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul J-M, Alboresi A, Weisshaar B, Lepiniec L (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 55(6):940–953

    Article  PubMed  CAS  Google Scholar 

  38. Gonzalez A (2009) Pigment loss in response to the environment: a new role for the WD/bHLH/MYB anthocyanin regulatory complex. New Phytol 182(1):1–3

    Article  PubMed  CAS  Google Scholar 

  39. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5(3):218–223

    Article  PubMed  CAS  Google Scholar 

  40. Wei Y-Z, Hu F-C, Hu G-B, Li X-J, Huang X-M, Wang H-C (2011) Differential expression of anthocyanin biosynthetic genes in relation to anthocyanin accumulation in the pericarp of Litchi chinensis Sonn. PLoS One 6(4):e19455

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Korea Atomic Energy Research Institute (KAERI) and the Ministry of Education, Science, and Technology (MEST), Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong Sub Kim.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sung, S.Y., Kim, S.H., Velusamy, V. et al. Comparative gene expression analysis in a highly anthocyanin pigmented mutant of colorless chrysanthemum. Mol Biol Rep 40, 5177–5189 (2013). https://doi.org/10.1007/s11033-013-2620-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-013-2620-5

Keywords