Skip to main content
SpringerLink
Log in

An active hAT transposable element causing bud mutation of carnation by insertion into the flavonoid 3′-hydroxylase gene

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

Abstract

The molecular mechanisms underlying spontaneous bud mutations, which provide an important breeding tool in carnation, are poorly understood. Here we describe a new active hAT type transposable element, designated Tdic101, the movement of which caused a bud mutation in carnation that led to a change of flower color from purple to deep pink. The color change was attributed to Tdic101 insertion into the second intron of F3′H, the gene for flavonoid 3′-hydroxylase responsible for purple pigment production. Regions on the deep pink flowers of the mutant can revert to purple, a visible phenotype of, as we show, excision of the transposable element. Sequence analysis revealed that Tdic101 has the characteristics of an autonomous element encoding a transposase. A related, but non-autonomous element dTdic102 was found to move in the genome of the bud mutant as well. Its mobilization might be the result of transposase activities provided by other elements such as Tdic101. In carnation, therefore, the movement of transposable elements plays an important role in the emergence of a bud mutation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abe Y, Tera M, Sasaki N, Okamura M, Umemoto N, Momose M, Kawahara N, Kamakura H, Goda Y, Nagasawa K, Ozeki Y (2008) Detection of 1-O-malylglucose: pelargonidin 3-O-glucose-6′′-O-malyltransferase activity in carnation (Dianthus caryophyllus). Biochem Biophys Res Commun 373:473–477

    Article  PubMed  CAS  Google Scholar 

  • Azuma A, Kobayashi S, Goto-Yamamoto N, Shiraishi M, Mitani N, Yakushiji H, Koshita Y (2009) Color recovery in berries of grape (Vitis vinifera L.) ‘Benitaka’, a bud sport of ‘Italia’, is caused by a novel allele at the VvmybA1 locus. Plant Sci 176:470–478

    Article  CAS  Google Scholar 

  • Bloor SJ (1998) A macrocyclic anthocyanin from red mauve carnation flowers. Phytochemistry 49:225–228

    Article  CAS  Google Scholar 

  • Britsch L, Dedio J, Saedler H, Forkmann G (1993) Molecular characterization of flayanone 3β-hydroxylases. Eur J Biochem 217:745–754

    Article  PubMed  CAS  Google Scholar 

  • Brugliera F, Barri-Rewell G, Holton TA, Mason JG (1999) Isolation and characterization of a flavonoid 3′-hydroxylase cDNA clone corresponding to the Ht1 locus of Petunia hybrida. Plant J 19:441–451

    Article  PubMed  CAS  Google Scholar 

  • Carpenter R, Martin C, Coen ES (1987) Comparison of genetic behaviour of the transposable element Tam3 at two unlinked pigment loci in Antirrhinum majus. Mol Gen Genet 207:82–89

    Article  CAS  Google Scholar 

  • Coen ES, Carpenter R, Martin C (1986) Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell 47:285–296

    Article  PubMed  CAS  Google Scholar 

  • Dawe RK, Freeling M (1991) Cell lineage and its consequences in higher plants. Plant J 1:3–8

    Article  Google Scholar 

  • Fujino K, S-n Hashida, Ogawa T, Natsume T, Uchiyama T, Mikami T, Kishima Y (2011) Temperature controls nuclear import of Tam3 transposase in Antirrhinum. Plant J 65:146–155

    Article  PubMed  CAS  Google Scholar 

  • Fukui Y, Tanaka Y, Kusumi T, Iwashita T, Nomoto K (2003) A rationale for the shift in colour towards blue in transgenic carnation flowers expressing the flavonoid 3′,5′-hydroxylase gene. Phytochemistry 63:15–23

    Article  PubMed  CAS  Google Scholar 

  • Geissman TA, Mehlquist GA (1947) Inheritance in the carnation, Dianthus caryophyllus: the chemistry of flower color variation. Genetics 32:410–433

    CAS  Google Scholar 

  • Harrison BJ, Fincham JRS (1968) Instability at the Pal locus in Antirrhinum majus 3. A gene controlling mutation frequency. Heredity 23:67–72

    Article  Google Scholar 

  • Hashida S-N, Uchiyama T, Martin C, Kishima Y, Sano Y, Mikami T (2006) The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell 18:104–118

    Article  PubMed  CAS  Google Scholar 

  • Hehl R, Nacken WK, Krause A, Saedler H, Sommer H (1991) Structural analysis of Tam3, a transposable element from Antirrhinum majus, reveals homologies to the Ac element from maize. Plant Mol Biol 16:369–371

    Article  PubMed  CAS  Google Scholar 

  • Huala E, Sussex IM (1993) Determination and cell interactions in reproductive meristems. Plant Cell 5:1157–1165

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Inagaki Y, Hisatomi Y, Iida S (1996) Somatic mutations caused by excision of the transposable element, Tpn1, from the DFR gene for pigmentation in sub-epidermal layer of periclinally chimeric flowers of Japanese morning glory and their germinal transmission to their progeny. Theoret Appl Genet 92:499–504

    Article  CAS  Google Scholar 

  • Itoh Y, Higeta D, Suzuki A, Yoshida H, Ozeki Y (2002) Excision of transposable elements from the chalcone isomerase and dihydroflavonol 4-reductase genes may contribute to the variegation of the yellow-flowered carnation (Dianthus caryophyllus). Plant Cell Physiol 43:578–585

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Liu Q, Zhu A, Chai L, Zhou W, Yu K, Ding J, Xu J, Deng X (2009) Transcriptome analysis of a spontaneous mutant in sweet orange [Citrus sinensis (L.) Osbeck] during fruit development. J Exp Bot 60:801–813

    Article  PubMed  CAS  Google Scholar 

  • Mato M, Onozaki T, Ozeki Y, Higeta D, Itoh Y, Yoshimoto Y, Ikeda H, Yoshida H, Shibata M (2000) Flavonoid biosynthesis in white-flowered Sim carnations (Dianthus caryophyllus). Sci Hortic 84:333–347

    Article  CAS  Google Scholar 

  • Matsuba Y, Sasaki N, Tera M, Okamura M, Abe Y, Okamoto E, Nakamura H, Funabashi H, Takatsu M, Saito M, Matsuoka H, Nagasawa K, Ozeki Y (2010) A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 22:3374–3389

    Article  PubMed  CAS  Google Scholar 

  • Mérai Z, Benkovics AH, Nyikó T, Debreczeny M, Hiripi L, Kerényi Z, Kondorosi É, Silhavy D (2013) The late steps of plant nonsense-mediated mRNA decay. Plant J 73:50–62

    Article  Google Scholar 

  • Nakayama M, Koshioka M, Yoshida H, Kan Y, Fukui Y, Koike A, Yamaguchi M (2000) Cyclic malyl anthocyanins in Dianthus caryophyllus. Phytochemistry 55:937–939

    Article  PubMed  CAS  Google Scholar 

  • Nishihara M, Hikage T, Yamada E, Nakatsuka T (2011) A single-base substitution suppresses flower color mutation caused by a novel miniature inverted-repeat transposable element in gentian. Mol Genet Genomics 286:371–382

    Article  PubMed  CAS  Google Scholar 

  • Nishizaki Y, Matsuba Y, Okamoto E, Okamura M, Ozeki Y, Sasaki N (2011) Structure of the acyl-glucose-dependent anthocyanin 5-O-glucosyltransferase gene in carnations and its disruption by transposable elements in some varieties. Mol Genet Genomics 286:383–394

    Article  PubMed  CAS  Google Scholar 

  • Ogata J, Itoh Y, Ishida M, Yoshida H, Ozeki Y (2004) Cloning and heterologous expression of cDNAs encoding flavonoid glucosyltransferases from Dianthus caryophyllus. Plant Biotechnol 21:367–375

    Article  CAS  Google Scholar 

  • Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957

    PubMed  CAS  Google Scholar 

  • Satina S, Blakeslee AF, Avery AG (1940) Demonstration of the three germ layers in the shoot apex of datura by means of induced polyploidy in periclinal chimeras. Am J Bot 27:895–905

    Article  Google Scholar 

  • Shibata M, Kishimoto S, Hirai M, Aida R, Ikeda I (1998) Analysis of the periclinal chimeric structure of chrysanthemum sports by random amplified polymorphic DNA. Acta Hortic 454:347–353

    CAS  Google Scholar 

  • Spribille R, Forkmann G (1982) Chalcone synthesis and hydroxylation of flavonoids in 3′-position with enzyme preparations from flowers of Dianthus caryophyllus L. (carnation). Planta 155:176–182

    Article  CAS  Google Scholar 

  • Sussex IM (1989) Developmental programming of the shoot meristem. Cell 56:225–229

    Article  PubMed  CAS  Google Scholar 

  • Toda K, Yang D, Yamanaka N, Watanabe S, Harada K, Takahashi R (2002) A single-base deletion in soybean flavonoid 3′-hydroxylase gene is associated with gray pubescence color. Plant Mol Biol 50:187–196

    Article  PubMed  CAS  Google Scholar 

  • Ueyama Y, Suzuki K-i, Fukuchi-Mizutani M, Fukui Y, Miyazaki K, Ohkawa H, Kusumi T, Tanaka Y (2002) Molecular and biochemical characterization of torenia flavonoid 3′-hydroxylase and flavone synthase II and modification of flower color by modulating the expression of these genes. Plant Sci 163:253–263

    Article  CAS  Google Scholar 

  • Van Harten A (2002) Mutation breeding of vegetatively propagated ornamentals. In: Vainstein A (ed) Breeding for ornamentals: classical and molecular approaches. Kluwer Academic Publishers, Dordrecht, pp 105–128

    Chapter  Google Scholar 

  • Walbot V, Warren C (1988) Regulation of Mu element copy number in maize lines with an active or inactive mutator transposable element system. Mol Gen Genet 211:27–34

    Article  PubMed  CAS  Google Scholar 

  • Walker A, Lee E, Robinson S (2006) Two new grape cultivars, bud sports of Cabernet Sauvignon bearing pale-coloured berries, are the result of deletion of two regulatory genes of the berry colour locus. Plant Mol Biol 62:623–635

    Article  PubMed  CAS  Google Scholar 

  • Wolff K (1996) RAPD analysis of sporting and chimerism in chrysanthemum. Euphytica 89:159–164

    Article  CAS  Google Scholar 

  • Yakushiji H, Kobayashi S, Goto-Yamamoto N, Tae Jeong S, Sueta T, Mitani N, Azuma A (2006) A skin color mutation of grapevine, from black-skinned pinot noir to white-skinned pinot blanc, is caused by deletion of the functional VvmybA1 allele. Biosci Biotechnol Biochem 70:1506–1508

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Akimoto H, Yamaguchi M, Shibata M, Habu Y, Iida S, Ozeki Y (2004) Alteration of methylation profiles in distinct cell lineages of the layers during vegetative propagation in carnations (Dianthus caryophyllus). Euphytica 135:247–253

    Article  CAS  Google Scholar 

  • Yoshimoto Y, Higeta D, Ito Y, Yoshida H, Hasebe M, Ozeki Y (2000) Isolation and characterization of a cDNA for phenylalanine ammonia-lyase (PAL) from Dianthus caryophyllus (carnation). Plant Biotechnol 17:325–329

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank to Takayasu Hirosawa, Hiroshi Okawa and Noboru Onishi for helpful discussions. This work was partly supported by a grant from the “Technical Development Program for Making Agribusiness in the Form of Utilizing the Concentrated Know-how from the Private Sector” of the Ministry of Agriculture, Forestry and Fisheries JAPAN.

Author information

Authors and Affiliations

  1. Central Laboratories for Key Technologies, Kirin Co., Ltd, Fukuura 1-13-5, Yokohama, Kanagawa, 236-0004, Japan

    Masaki Momose, Naoyuki Umemoto & Toshihiro Toguri

  2. Department of Biotechnology and Life Science, Faculty of Engineering, Tokyo University of Agriculture and Technology, Naka-cho 2-24-16, Koganei, Tokyo, 184-8588, Japan

    Yoshio Itoh & Yoshihiro Ozeki

  3. Institute of Floricultural Science, National Agriculture and Food Research Organization, Fujimoto 2-1, Tsukuba, Ibaraki, 305-8519, Japan

    Masayoshi Nakayama

Authors
  1. Masaki Momose
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayoshi Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoshio Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoyuki Umemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Toshihiro Toguri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshihiro Ozeki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masaki Momose.

Additional information

Communicated by M.-A. Grandbastien.

Yoshio Itoh: deceased.

Nucleotide sequence data reported are deposited in the DDBJ database under the accession numbers AB731559, AB731560, AB731561 and AB731562.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 56 kb)

Supplementary material 2 (PPT 1801 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Momose, M., Nakayama, M., Itoh, Y. et al. An active hAT transposable element causing bud mutation of carnation by insertion into the flavonoid 3′-hydroxylase gene. Mol Genet Genomics 288, 175–184 (2013). https://doi.org/10.1007/s00438-013-0742-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0742-z

Keywords

Search

Navigation