Skip to main content
Log in

Genome-Wide Analysis of the R2R3 MYB Subfamily Genes in Lotus (Nelumbo nucifera)

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

MYB superfamily is one of the most abundant transcription factors in plants, which are involved in many physiological and biochemical processes. Among them, R2R3 MYB might be the most widely studied subfamily. Here, we characterized the gene structures, expressional patterns, and potential functions of 116 R2R3 MYB genes in a genome-wide manner in lotus (Nelumbo nucifera). Compared with those in Arabidopsis and grape, the lotus R2R3 MYB genes are conserved in exon’s number and length. Most of them constitute three exons and two introns with the first two exons being highly conserved in their length. According to the structure of exon and DNA-binding domain-imperfect repeat (R), these R2R3 MYB genes were classified into four groups. The expression of 13 candidate MYB genes that are related to flavonoid biosynthesis was analyzed in lotus different tissues. One gene expresses highly in all tissues and might positively regulate common flavonoid biosynthesis. Two genes might positively regulate anthocyanin and proanthocyanidin biosynthesis, respectively, resulting in the pigmentation of flower and seed. While five members that are similar to Zm38 are expressed lowly in different tissues. This genome-wide analysis of R2R3 MYB genes in lotus may provide more comprehensive insights on the structure and function of this gene family, and hence contribute a lot to plant’s genetic engineering in improving the colorization of flowers or other tissues.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /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

References

  • Abeynayake SW, Panter S, Chapman R, Webster T, Rochfort S, Mouradov A, Spangenberg G (2011) Biosynthesis of proanthocyanidins in white clover flowers: cross talk within the flavonoid pathway. Plant Physiol 158:666–678

    Article  PubMed  PubMed Central  Google Scholar 

  • Albert NW, Lewis DH, Zhang H, Schwinn KE, Jameson PE, Davies KM (2011) Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. Plant J 65:771–784

    Article  CAS  PubMed  Google Scholar 

  • Albert NW, Davies KM, Lewis DH, Zhang H, Montefiori M, Brendolise C, Boase MR, Ngo H, Jameson PE, Schwinn KE (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26:962–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Appelhagen I, Jahns O, Bartelniewoehner L, Sagasser M, Weisshaar B, Stracke R (2011a) Leucoanthocyanidin Dioxygenase in Arabidopsis thaliana: Characterization of mutant alleles and regulation by MYB–BHLH–TTG1 transcription factor complexes. Gene 484:61–68

  • Appelhagen I, Lu G-H, Huep G, Schmelzer E, Weisshaar B, Sagasser M (2011b) TRANSPARENT TESTA1 interacts with R2R3-MYB factors and affects early and late steps of flavonoid biosynthesis in the endothelium of Arabidopsis thaliana seeds. Plant J 67:406–419

  • Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP (2007) The Grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143:1347–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavallini E, Zenoni S, Flavia G, Zamboni A, Avesani L, Tornielli GB (2013) Functional diversification of grapevine MYB5a and MYB5b in the control of flavonoid biosynthesis in a petunia anthocyanin regulatory mutant. Plant Cell Physiol 55:517–534

    Article  PubMed  Google Scholar 

  • Chen Y, Yang X, He K, Liu M, Li J, Gao Z, Lin Z, Zhang Y, Wang X, Qiu X (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  Google Scholar 

  • Chen S, Xiang Y, Deng J, Liu YL, Li SH (2013) Simultaneous analysis of anthocyanin and non-anthocyanin flavonoid in various tissues of different lotus (Nelumbo nucifera) cultivars by HPLC-DAD-ESI-MSn. PLoS One 8:e62291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Czemmel S, Heppel SC, Bogs J (2012) R2R3 MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 249:109–118

    Article  CAS  Google Scholar 

  • Deng J, Chen S, Yin X, Wang K, Liu Y, Li S, Yang P (2013) Systematic qualitative and quantitative assessment of anthocyanins, flavones and flavonols in the petals of 108 lotus (Nelumbo nucifera) cultivars. Food Chem 139:307–312

    Article  CAS  PubMed  Google Scholar 

  • Dias AP (2003) Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol 131:610–620

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Espley RV, Brendolise C, Chagne D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, Allan AC (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21:168–183

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Franken P, Schrell S, Peterson P, Saedler H, Wienand U (1994) Molecular analysis of protein domain function encoded by the myb-homologous maize genes C1, Zm I and Zm 38. Plant J 6:21–30

    Article  CAS  PubMed  Google Scholar 

  • Klempnauer K, Gonda TJ (1982) Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell 31:453–463

    Article  CAS  PubMed  Google Scholar 

  • Koyama K, Numata M, Nakajima I, Goto-Yamamoto N, Matsumura H, Tanaka N (2014) Functional characterization of a new grapevine MYB transcription factor and regulation of proanthocyanidin biosynthesis in grapes. J Exp Bot 65:4433–4449

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li A, Shao X, Yan F (2009) The study of extraction process of polyphenol in Lotus Root. China Food Additives 5:80–84 (in Chinese)

    Google Scholar 

  • Martin C, Prescott A, Mackay S, Bartlett J, Vrijlandt E (1991) Control of anthocyanin biosynthesis in flowers of Antirrhinurn majus. Planl J 1:37–49

    Article  CAS  Google Scholar 

  • Matus J, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83

    Article  PubMed  PubMed Central  Google Scholar 

  • Ming R, VanBuren R, Liu Y, Yang M, Han Y, Li L-T, Zhang Q, Kim M-J, Schatz MC, Campbell M, Li J, Bowers JE, Tang H, Lyons E, Ferguson AA, Narzisi G, Nelson DR, Blaby-Haas CE, Gschwend AR, Jiao Y, Der JP, Zeng F, Han J, Min X, Hudson KA, Singh R, Grennan AK, Karpowicz SJ, Watling JR, Ito K, Robinson SA, Hudson ME, Yu Q, Mockler TC, Carroll A, Zheng Y, Sunkar R, Jia R, Chen N, Arro J, Wai C, Wafula E, Spence A, Han Y, Xu L, Zhang J, Peery R, Haus MJ, Xiong W, Walsh JA, Wu J, Wang M-L, Zhu YJ, Paull RE, Britt AB, Du C, Downie SR, Schuler MA, Michael TP, Long SP, Ort DR, William Schopf J, Gang DR, Jiang N, Yandell M, dePamphilis CW, Merchant SS, Paterson AH, Buchanan BB, Li S, Shen-Miller J (2013) Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 14:R41

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukherjee PK, Mukherjee D, Maji AK, Rai S, Heinrich M (2009) The sacred lotus (Nelumbo nucifera)—phytochemical and therapeutic profile. J Pharm Pharmacol 61:407–422

    Article  CAS  PubMed  Google Scholar 

  • Nemie-Feyissa D, Olafsdottir SM, Heidari B, Lillo C (2014) Nitrogen depletion and small R3-MYB transcription factors affecting anthocyanin accumulation in Arabidopsis leaves. Phys Chem Chem Phys 98:34–40

    CAS  Google Scholar 

  • Oberholzer V, Durbin M, Clegg M (2000) Proceedings of Fukuoka International Symposium on Population Genetics. Genes Genet Syst 75:1–16

    Article  CAS  PubMed  Google Scholar 

  • Quattrocchio F (1993) Regulatory genes controlling anthocyanin pigmentation Are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5:1497–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen X, Zhao K, Liu L, Zhang H, Liao X, Wang Q, Guo X, Li F, LI T (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55:517–534

    Article  Google Scholar 

  • Stracke R, Werber MWB (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Verdier J, Zhao J, Torres-Jerez I, Ge S, Liu S, He X, Mysore K, Dixon R, Udvardi M (2012) MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. PNAS 31:1766–1771

    Article  Google Scholar 

  • Vogt T (2009) Phenylpropanoid biosynthesis. Mol Plant 3:2–20

    Article  PubMed  Google Scholar 

  • Wang Y, Fan G, Liu Y, Sun F, Shi C, Liu X, Peng J, Chen W, Huang X, Cheng S, Liu Y, Liang X, Zhu H, Bian C, Zhong L, Lv T, Dong H, Liu W, Zhong X, Chen J, Quan Z, Wang Z, Tan B, Lin C, Mu F, Xu X, Ding Y, Guo A-Y, Wang J, Ke W (2013) The sacred lotus genome provides insights into the evolution of flowering plants. Plant J 76:557–567

    Article  CAS  PubMed  Google Scholar 

  • Woodger FJ, Millar A, Murray F, Jacobsen JV, Gubler F (2003) The role of GAMYB transcription factors in GA-regulated gene expression. J Plant Growth Reg 22:176–184

    Article  CAS  Google Scholar 

  • Xu W, Grain D, Bobet S, Le Gourrierec J, Thévenin J, Kelemen Z, Lepiniec L, Dubos C (2014) Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed. New Phytol 202:132–144

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Li JH, Xin HP, Wang N, Guan L, Wu BH, Li SH (2013) Anthocyanin profile and gene expression in berry skin of two red Vitis vinifera grape cultivars that are sunlight dependent versus sunlight independent. Australian J Grape Wine Res 19:238–248

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by The Knowledge Innovation Project grant (no. Y455421Z02) of the Chinese Academy of Sciences to Pingfang Yang.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mei Yang or Pingfang Yang.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary file 1

List of 116 lotus R2R3 MYB genes with annotations, positions in the genome, predicted protein length, exon lengths, and expression profile in four different tissues. (GIF 47 kb)

High-resolution image (TIF 1644 kb)

Supplementary file 2

Multiple alignments of 20 typic R2R3 MYB DNA-binding domains from Arabidopsis and 10 MYB R2R3 domains from lotus MYB proteins. The blue and yellow boxes represented the R2 and R3 repeats, respectively. (XLS 75 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deng, J., Li, M., Huang, L. et al. Genome-Wide Analysis of the R2R3 MYB Subfamily Genes in Lotus (Nelumbo nucifera). Plant Mol Biol Rep 34, 1016–1026 (2016). https://doi.org/10.1007/s11105-016-0981-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-016-0981-3

Keywords

Navigation