Skip to main content
Log in

A new MADS-box gene (IbMADS10) from sweet potato (Ipomoea batatas (L.) Lam) is involved in the accumulation of anthocyanin

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

A new MADS-box gene designated as IbMADS10 was cloned and its expression was characterized from sweet potato (Ipomoea batatas (L.) Lam.) cv. Beniazuma. The deduced amino acid sequence of the gene indicated high homology with members of the MADS-box family of transcription factors. IbMADS10 shares high amino acid sequence similarity with the DEFH28 of Antirrhinum majus (64%) and with BpMADS4 of Betula pendula (61%) of the SQUA subfamily. Southern blot analysis revealed that the IbMADS10 is present in one or low copy number in the sweet potato genome. The gene is specifically expressed in the pigmented tissues such as in the flower bud, in the pink and in red roots, and hence, it was speculated that the IbMADS10 gene might be correlated with anthocyanin biosynthesis in sweet potato. RNA blot expression of the anthocyanin biosynthesis genes encoding for CHS, CHI, F3H, DFR, ANS and UFTG carried out in the tissues where the IbMADS10 gene was expressed revealed similar transcript levels in all tissues where the IbMADS10 gene is highly expressed, indicating that the IbMADS10 gene is highly correlated with the anthocyanin biosynthesis genes. Another important aspect is the pigmented phenotypes of transgenic calli that ectopically express the IbMADS10 gene, thereby supporting its involvement in the developmental regulation of pigment formation. Tissue printing result further strengthens the hypothesis that the IbMADS10 gene is indeed involved in anthocyanin pigmentation in sweet potato. As the purpose of the IbMADS10 gene is pigmentation, its function, therefore, resembles that of the transparent testa (tt) genes of Arabidopsis.

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

Similar content being viewed by others

References

  • Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pamplona L, Marinez-Castilla L, Yanofsky MF (2000) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Nat’l Acad Sci 97:5328–5333

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Kaufmann K, Freialdenhoven A, Vincent C, Li MA, Saedler H, Theiβen G (2002) A novel MADS-box gene subfamily with sister-group relationship to class B floral homeotic genes. Mol Gen Genomics 266:942–950

    Article  CAS  Google Scholar 

  • Becker A, Theiβen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Winter KU, Meyer B, Saedler H, Theiβen G (2000) MADS-box gene diversity in seed plants 300 million years ago. Mol Biol Evol 17:1425–1434

    PubMed  CAS  Google Scholar 

  • 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 111:1059–1066

    PubMed  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney SP (1993) A simple and efficient method for isolating RNA from fine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Coen ES, EM Meyerrowitz (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination and longevity in Arabidopsis. Plant Physiol 122:403–413

    Article  PubMed  CAS  Google Scholar 

  • Debeaujon I, Peeters AJM, Leon-Kloosterziel KM, Koornneef M (2001) The TRANSPARENT TESTA 12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13:853–872

    Article  PubMed  CAS  Google Scholar 

  • de Vetten N, Quattrocchio F, Mol J, Koes R (1997) The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants and animals. Genes Dev 11:1422–1434

    Article  PubMed  Google Scholar 

  • Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, Pelletier G, Delseny M (1999) The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J 19:387–398

    Article  PubMed  CAS  Google Scholar 

  • Feinbaum RL, Ausubel FM (1988) Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol Cell Biol 8:1985–1992

    PubMed  CAS  Google Scholar 

  • Focks N, Sagasser M, Weisshaar B, Benning C (1999) Characterization of tt15, a novel transparent testa mutant of Arabidopsis thaliana (L.) heyn. Planta 208:352–357

    Article  PubMed  CAS  Google Scholar 

  • Goodrich J, Carpenter R, Coen ES (1992) A common gene regulates pigmentation pattern in diverse plant species. Cell 68:955–964

    Article  PubMed  CAS  Google Scholar 

  • Hrazdina G, Parsons GF, Mattick LR (1984) Physiological and biochemical events during development and maturation of grape berries. Amer J Enol Vitic 35:220–227

    CAS  Google Scholar 

  • Hu J, Nakatani M, Lalusin AG, Kuranouchi T, Fujimura T (2003) Genetic analysis of sweetpotato and wild relatives using inter-simple sequence repeats (ISSRs). Breeding Sci 53:297–304

    Article  CAS  Google Scholar 

  • Huijser P, Lein J, Lonnig WE, Meijer H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11:1239–1249

    PubMed  CAS  Google Scholar 

  • Immink RGH, Hannapel DJ, Ferrario S, Busscher M, Franken J, Lookeren-Campagne MM, Angement GC (1999) A petunia MADS-box gene involved in the transition from vegetative to reproductive development. Development 126:5117–5126

    PubMed  CAS  Google Scholar 

  • Kim SH, Mizuno K, Fujimura T (2002) Isolation of MADS-box genes from sweetpotato (Ipomoea batatas (L.) Lam) expressed specifically in vegetative tissues. Plant Cell Physiol 43(3):314–322

    Article  PubMed  CAS  Google Scholar 

  • Kitamura S, Shikazono, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114

    Article  PubMed  CAS  Google Scholar 

  • Koes R, Quattrocchio R, Mol J (1994) The flavonoid biosynthetic pathway in plants:function and evolution. BioEssays 16:123–132

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Kofuji R, Sumikawa N, Yamazaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003) Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20(12):1963–1977

    Article  PubMed  CAS  Google Scholar 

  • Konczak-Islam I, Yoshinaga M, Nakatani M, Yamakawa O (2000) Establishment and characteristics of an anthocyanin-producing cell line from sweetpotato storage root. Plant Cell Rep 19:472–477

    Article  CAS  Google Scholar 

  • Koornneef M (1990) Mutations affecting the testa colour in Arabidopsis. Arabid Inf Serv 27:1–4

    Google Scholar 

  • Ludwig SR, Habera LF, Dellaporta SL, Wessler SR (1989) Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc Nat’l Acad Sci 86:7092–7096

    Article  PubMed  CAS  Google Scholar 

  • Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8:745–756

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Jin H, Schinn K (2001) Mechanisms and applications of transcriptional control of phenylpropanoid metabolism. In: Romeo JT, Saunders JA, Matthew BF (eds) Regulation of Phytochemicals by Molecular Techniques. Elsevier Science Ltd, Oxford, pp 155–170

    Google Scholar 

  • Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3:212–217

    Article  Google Scholar 

  • Munster T, Pahnke J, diRosa A, Kim J, Martin W, Saedler H, Theiβen G (1997) Floral homeotic genes were recruited from homologous MADS-box genes pre-existing in the common ancestor of ferns and seed plants. Proc Nat’l Acad Sci 94:2415–2420

    Article  PubMed  CAS  Google Scholar 

  • Nesi N, Debeaujon I, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12:1863–1878

    Article  PubMed  CAS  Google Scholar 

  • Nesi N, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R3R3 MYB domain protein that acts as a key determinant for the proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114

    Article  PubMed  CAS  Google Scholar 

  • Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The TRANSPARENT TESTA 16 locus encodes the Arabidopsis Bsister MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:2463–2479

    Article  PubMed  CAS  Google Scholar 

  • Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195

    Article  PubMed  CAS  Google Scholar 

  • Otani M, Shimada T, Kimura T, Saito A (1998) Transgenic plant production from embryogenic callus of sweetpotato (Ipomoea batatas (L.) Lam) using Agrobacterium tumefaciens. Plant Biotechnol 15(1):11–16

    CAS  Google Scholar 

  • Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem 61:1053–1095

    Article  PubMed  CAS  Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551

    Article  PubMed  CAS  Google Scholar 

  • Pelletier MK, Shirley BW (1996) Analysis of flavone 3-hydroxylase in Arabidopsis seedlings: coordinate regulation with chalcone synthase and chalcone isomerase. Plant Physiol 111:339–345

    Article  PubMed  CAS  Google Scholar 

  • Pelletier MK, Murrell JR, Shirley BW (1997) Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis. Plant Physiol 113:1437–1445

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD (1998) The molecular evolution of development. Bioessays 20:700–711

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356

    PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444

    Article  PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing JF, van der Woude K, Mol JNM, Koes RE (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  PubMed  CAS  Google Scholar 

  • Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Proc Nat’l Acad Sci 93:4793–4798

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101

    Article  PubMed  CAS  Google Scholar 

  • Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

    Article  PubMed  CAS  Google Scholar 

  • Sagasser M, Lu G, Hahlbrock K, Weisshaar B (2002) A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev 16:138–149

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular Cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, NY

    Google Scholar 

  • Schoenbohm C, Martens S, Eder C, Forkmann G, Weisshaar B (2000) Identification of the Arabidopsis thaliana flavonoid 3’hydroxylase gene and functional expression of the encoded P450 enzyme. Biol Chem 381:749–753

    Article  PubMed  CAS  Google Scholar 

  • Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936

    Article  PubMed  CAS  Google Scholar 

  • Shirley BW, Hanley S, Goodman HM (1992) Effects of ionizing radiation on a plant genome: analysis of two arabidopsis mutant deficient in flavonoid biosynthesis. Plant Cell 4:333–347

    Article  PubMed  CAS  Google Scholar 

  • Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM (1995) Analysis of Arabidopsis mutant deficient in flavonoid biosynthesis. Plant J 8:659–671

    Article  PubMed  CAS  Google Scholar 

  • Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13

    Article  PubMed  CAS  Google Scholar 

  • Smyth D (2000) A reverse trend: MADS functions revealed. Trends Plant Sci 5:315–317

    Article  PubMed  CAS  Google Scholar 

  • Somers TC (1976) Pigment development during the ripening of grape. Vitis 14:269–277

    CAS  Google Scholar 

  • Spelt C, Quattrocchio F, Mol JNM, Koes R (2000) Anthocyanin 1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12:1619–1631

    Article  PubMed  CAS  Google Scholar 

  • Theiβen G, Strater T, Fisher A, Saedler H (1995) Structural characterization of chromosomal location and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene 156:155–166

    Article  PubMed  Google Scholar 

  • Theiβen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516

    PubMed  Google Scholar 

  • Theiβen G, Becker A, di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box gene subfamilies in the morphological evolution of eukaryotes. Plant Mol Biol 42:115–149

    Article  PubMed  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  PubMed  CAS  Google Scholar 

  • Wilson LA (1982) Tuberization in sweetpotato (Ipomoea batatas (L) Lam.). In: RL Villareal and TD Griggs (eds) “Sweetpotato” Proceedings of the 1st International Symposium, AVRDC: Taiwan, China, pp 79–93

  • Winkel-Shirley B (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Wisman E, Hartmann U, Sagasser M, Baumann E, Palme K, Hahlbrock K, Saedler H, Weisshaar B (1998) Knock out mutants from En-1 mutagenized Arabidopsis thaliana population generate phenylpropanoid biosynthesis phenotypes. Proc Nat’l Acad Sci 95:12432–12437

    Article  PubMed  CAS  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Fieldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39

    Article  PubMed  CAS  Google Scholar 

  • Ye ZH, Varner JE (1991) Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell 3:23–37

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga M, Tanaka M, Nakatani M (2000) Changes in anthocyanin content and composition of developing storage root of purple-fleshed sweetpotato (Ipomoea batatas (L) Lam.). Breeding Sci 50:59–64

    CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the Japan Government for granting a Monbusho Scholarship to A.G. Lalusin. Grateful appreciation is also extended to Drs. T.P.N. Talorete and R. Laza for a critical review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonio G. Lalusin.

Additional information

Communicated by G. Jürgens

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lalusin, A.G., Nishita, K., Kim, SH. et al. A new MADS-box gene (IbMADS10) from sweet potato (Ipomoea batatas (L.) Lam) is involved in the accumulation of anthocyanin. Mol Genet Genomics 275, 44–54 (2006). https://doi.org/10.1007/s00438-005-0080-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-005-0080-x

Keywords

Navigation