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Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross

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Abstract

Orchids are one of the most unique and evolved of flowering plants, with many being valuable floricultural crops. Spatial localization of pigments within the flower of the commercially important bi-color Oncidium Gower Ramsey demonstrated a mixture of carotenoids and anthocyanins concentrated in the adaxial epidermis. Chromatography identified the predominant yellow pigment to be an equal mixture of all-trans and 9-cis isomers of violaxanthin, with esterification specific to the 9-cis isomer. Red ornamentation was comprised of the anthocyanins cyanidin and its methylated derivate, peonidin. Five key pigment biosynthesis genes encoding dihydroflavonol 4-reductase (DFR), phytoene synthase (PSY), phytoene desaturase, carotenoid isomerase, and the downstream 9-cis epoxycarotenoid dioxygenase were isolated and their expression profiles determined. Northern analyses showed both phytoene desaturase and carotenoid isomerase expression to be up-regulated in floral tissue relative to leaves whereas PSY was not. Three closely related DFR genes were isolated, including one with an insertion in the 3′ coding region. DFR expression occurred throughout flower development in Oncidium, unlike in Dendrobium and Bromheadia orchids. A number of the isolated anthocyanin and carotenoid genes showed variations due to insertion events. These findings raise questions about the genetic stability in interspecific crosses in orchids, such as the tri-specific Oncidium Gower Ramsey.

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Abbreviations

DFR:

Dihydroflavonol 4-reductase

DHK:

Dihydrokaempferol

DHQ:

Dihydroquercetin

DHM:

Dihydromyricetin

F3′H:

Flavonoid 3′-hydroxylase

F3′5′H:

Flavonoid 3′, 5′-hydroxylase

ocrtISO:

Oncidium carotenoid isomerase

oDFR:

Oncidium dihydroflavonol 4-reductase

oNCED:

Oncidium 9-cis epoxycarotenoid dioxygenase

oPDS:

Oncidium phytoene desaturase

oPSY:

Oncidium phytoene synthase

PCR:

Polymerase chain reaction

RACE:

Rapid amplification of cDNA ends

RT-PCR:

Reverse transcription and polymerase chain reaction

References

  • Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226

    Article  PubMed  CAS  Google Scholar 

  • Al-Babili S, Hugueney P, Schledz M, Welsch R, Frohnmeyer H, Laule O, Beyer P (2000) Identification of a novel gene coding for neoxanthin synthase from Solanum tuberosum. FEBS Lett 485:168–172

    Article  PubMed  CAS  Google Scholar 

  • Arditti J (1992) Fundamentals of orchid biology. Wiley, New York

    Google Scholar 

  • Beld M, Martin C, Huits H, Stuitje AR, Gerats AGM (1989) Flavonoid synthesis in Petunia hybrida: partial characterization of dihydroflavonol-4-reductase genes. Plant Mol Biol 13:491–502

    Article  PubMed  CAS  Google Scholar 

  • Bouvier F, d’Harlingue A, Backhaus RA, Kumagai MH, Camara B (2000) Identification of neoxanthin synthase as a carotenoid cyclase paralog. Eur J Biochem 267:6346–6352

    Article  PubMed  CAS  Google Scholar 

  • Camara B (1993) Plant phytoene synthase complex: component enzymes, immunology, and biogenesis. Methods Enzymol 214:352–365

    Article  CAS  Google Scholar 

  • Camara B, Moneger R (1978) Free and esterified carotenoids in green and red fruits of Capsicum annuum. Phytochem 17:91–93

    Article  CAS  Google Scholar 

  • Charanasri U, Kamemoto H (1975) Additional chromosome numbers in Oncidium and allied genera. Am Orchid Soc Bull 44:686–691

    Google Scholar 

  • Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Cunningham FX (2002) Regulation of carotenoid synthesis and accumulation in plants. Pure Appl Chem 74:1409–1417

    Article  CAS  Google Scholar 

  • Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583

    Article  PubMed  CAS  Google Scholar 

  • Cunningham FX, Gantt E (2001) One ring or two? Determination of ring number in carotenoids by lycopene epsilon-cyclases. Proc Natl Acad Sci USA 98:2905–2910

    Article  PubMed  CAS  Google Scholar 

  • Davies KM (2000) Plant colour and fragrance. In: Verpoorte R, Alfermann AW (eds) Metabolic engineering of plant secondary metabolism. Kluwer, Dordrecht, pp 127–163

    Google Scholar 

  • Feldman M, Levy AA (2005) Allopolyploidy—a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258

    Article  PubMed  CAS  Google Scholar 

  • Fourney RM, Miyakoshi J, Day RS III, Paterson MC (1988) Northern blotting: efficient RNA staining and transfer. Focus 10:5–7

    Google Scholar 

  • Gau W, Ploschke H-J, Wünsche C (1983) Mass spectrometric identification of xanthophyll fatty acid esters from marigold flowers (Tagetes erecta) obtained by high performances liquid chromatography and Craig counter-current distribution. J Chromatogr 262:277–284

    Article  CAS  Google Scholar 

  • Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543:137–145

    Article  CAS  Google Scholar 

  • Giuliano G, Bartley GE, Scolnik PA (1993) Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379–387

    Article  PubMed  CAS  Google Scholar 

  • Griesbach RJ (1984) Effects of carotenoid-anthocyanin combinations on flower color. J Heredity 75:145–147

    CAS  Google Scholar 

  • Hahlbrock H, Griesbach H (1975) Biosynthesis of flavonoids. In: Harborne JB, Mabry TJ, Mabry H (eds) The flavonoids. Academic, San Diego, pp 866–915

    Google Scholar 

  • Helariutta Y, Elomaa P, Kotilainen M, Seppänen 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 22:183–193

    Article  PubMed  CAS  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  PubMed  CAS  Google Scholar 

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083

    Article  PubMed  CAS  Google Scholar 

  • Huits HSM, Gerats AGM, Kreike MM, Mol JNM, Koes RE (1994) Genetic control of dihydroflavonol 4-reductase gene expression in Petunia hybrida. Plant J 6:295–310

    Article  PubMed  CAS  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  PubMed  CAS  Google Scholar 

  • Johnson ET, Yi H, Shin B, Oh BJ, Cheong H, Choi G (1999) Cymbidium hybrida dihydroflavonol 4-reductase does not efficiently reduce dihydrokaempferol to produce orange pelargonidin-type anthocyanins. Plant J 19:81–85

    Article  PubMed  CAS  Google Scholar 

  • Johnson ET, Ryu S, Yi H, Shin B, Cheong H, Choi G (2001) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J 25:325–333

    Article  PubMed  CAS  Google Scholar 

  • Karvouni Z, John I, Taylor JE, Watson CF, Turner AJ, Grierson D (1995) Isolation and characterisation of a melon cDNA clone encoding phytoene synthase. Plant Mol Biol 27:1153–1162

    Article  PubMed  CAS  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659

    PubMed  CAS  Google Scholar 

  • Kuehnle AR (1997) Molecular biology of orchids. In: Arditti J, Pridgeon AM (eds) Orchid biology: reviews and perspectives VII. Kluwer, London, pp 75–115

    Google Scholar 

  • Kuehnle AR, Lewis DH, Markham KR, Mitchell KA, Davies KM, Jordan BR (1997) Floral flavonoids and pH in Dendrobium orchid species and hybrids. Euphytica 95:187–194

    Article  CAS  Google Scholar 

  • Liew CF, Loh CS, Goh CJ, Lim SH (1998) The isolation, molecular characterization and expression of dihydroflavonol 4-reductase cDNA in the orchid, Bromheadia finlaysoniana. Plant Sci 135:161–169

    Article  CAS  Google Scholar 

  • Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29:365–379

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Vega JM, Feldman M (1998) Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. II. Changes in low-copy coding DNA sequences. Genome 41:535–542

    Article  PubMed  CAS  Google Scholar 

  • Lowry JB, Keong SC (1973) A preliminary study of Malaysian orchid pigments. Malays J Sci 2:115–121

    CAS  Google Scholar 

  • Matsui S (1994) Floral carotenoids in species and hybrids of the Laeliinae. Lindleyana 9:213–217

    Google Scholar 

  • Matsui S, Nakamura M (1988) Distribution of flower pigments in perianth of Cattleya and allied genera. I. Species. J Jpn Soc Hortic Sci 57:222–232

    Google Scholar 

  • Moehs CP, Tian L, Osteryoung KW, DellaPenna D (2001) Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol Biol 45:281–293

    Article  PubMed  CAS  Google Scholar 

  • Moir WW, Moir MA (1982) Creating oncidiinae intergenerics. University of Hawaii Press, Honolulu

    Google Scholar 

  • Morris WL, Ducreux L, Griffiths DW, Stewart D, Davies HV, Taylor MA (2004) Carotenogenesis during tuber development and storage in potato. J Exp Bot 55:975–982

    Article  PubMed  CAS  Google Scholar 

  • Mudalige RM, Kuehnle AR (2004) Orchid biotechnology in production and improvement. HortSci 39:11–17

    Google Scholar 

  • Mudalige RM, Kuehnle AR, Amore TD (2003) Pigment distribution and epidermal cell shape in Dendrobium species and hybrids. HortSci 38:573–577

    Google Scholar 

  • Mudalige-Jayawickrama RG, Champagne MM, Hieber AD, Kuehnle AR (2005) Cloning and characterization of two anthocyanin biosynthetic genes from Dendrobium orchid. J Am Soc Hort Sci 130:611–618

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Planta 15:473–497

    Article  CAS  Google Scholar 

  • Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147

    Article  PubMed  CAS  Google Scholar 

  • Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361

    Article  PubMed  CAS  Google Scholar 

  • Rivas JD (1989) Reversed-phase high-performance liquid chromatographic separation of lutein and lutein fatty acid esters from marigold flower petal powder. J Chromatogr 464:442–447

    Article  PubMed  CAS  Google Scholar 

  • Sandmann G (2001) Genetic manipulation of carotenoid biosynthesis: strategies, problems and achievements. Trends Plant Sci 6:14–17

    Article  PubMed  CAS  Google Scholar 

  • Schiedt K, Liaaen-Jensen S (1995) Isolation and analysis. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids: isolation and analysis, vol 1A. Birkhauser Verlag, Berlin, pp 81–108

  • Schledz M, Al-Babili S, von LJ, Haubruck H, Rabbani S, Kleinig H, Beyer P (1996) Phytoene synthase from Narcissus pseudonarcissus: functional expression, galactolipid requirement, topological distribution in chromoplasts and induction during flowering. Plant J 10:781–792

    Article  PubMed  CAS  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  PubMed  CAS  Google Scholar 

  • Schwartz SH, Tan BC, McCarty DR, Welch W, Zeevaart JA (2003) Substrate specificity and kinetics for VP14, a carotenoid cleavage dioxygenase in the ABA biosynthetic pathway. Biochim Biophys Acta 1619:9–14

    PubMed  CAS  Google Scholar 

  • Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759

    Article  PubMed  CAS  Google Scholar 

  • Song K, Lu P, Tang K, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92:7719–7723

    Article  PubMed  CAS  Google Scholar 

  • Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  PubMed  CAS  Google Scholar 

  • Thammasiri K, Tang CS, Yamamoto HY, Kamemoto H (1986) Carotenoids and chlorophylls in yellow-flowered Dendrobium species. Lindleyana 1:215–218

    Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Xie D-Y, Jackson LA, Cooper JD, Ferreira D, Paiva NL (2004) Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol-4-reductase from Medicago truncatula. Plant Physiol 134:979–994

    Article  PubMed  CAS  Google Scholar 

  • Zhu C, Yamamura S, Koiwa H, Nishihara M, Sandmann G (2002) cDNA cloning and expression of carotenogenic genes during flower development in Gentiana lutea. Plant Mol Biol 48:277–285

    Article  PubMed  CAS  Google Scholar 

  • Zufall RA, Rausher MD (2004) Genetic changes associated with floral adaptation restrict future evolutionary potential. Nature 428:847–850

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the USDA Special Grants Program for Tropical and Subtropical Agriculture Research, grant number 2003-34135-13980 to A. D. Hieber and A. R. Kuehnle. We also would like to thank Prof. F. C. Chen for initial input, Dr. Teresita Amore for chromosome preparation, and also Prof. Harry Yamamoto for helpful discussions.

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  1. Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, 3190 Maile Way, St. John Rm 102, Honolulu, HI, 96822, USA

    A. David Hieber, Rasika G. Mudalige-Jayawickrama & Adelheid R. Kuehnle

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  1. A. David Hieber
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  2. Rasika G. Mudalige-Jayawickrama
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  3. Adelheid R. Kuehnle
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Correspondence to A. David Hieber.

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Hieber, A.D., Mudalige-Jayawickrama, R.G. & Kuehnle, A.R. Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross. Planta 223, 521–531 (2006). https://doi.org/10.1007/s00425-005-0113-z

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