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Chalcone synthase-like genes active during corolla development are differentially expressed and encode enzymes with different catalytic properties in Gerbera hybrida (Asteraceae)

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Abstract

Recent studies on chalcone synthase (CHS) and the related stilbene synthase (STS) suggest that the structure of chs-like genes in plants has evolved into different forms, whose members have both different regulation and capacity to code for different but related enzymatic activities. We have studied the diversity of chs-like genes by analysing the structure, expression patterns and catalytic properties of the corresponding enzymes of three genes that are active during corolla development in Gerbera hybrida. The expression patterns demonstrate that chs-like genes are representatives of three distinct genetic programmes that are active during organ differentiation in gerbera. Gchs1 and gchs3 code for typical CHS enzymes, and their gene expression pattern temporally correlates with flavonol (gchs1, gchs3) and anthocyanin (gchs1) synthesis during corolla development. Gchs2 is different. The expression pattern does not correlate with the pigmentation pattern, the amino acid sequence deviates considerably from the consensus of typical CHSs, and the catalytic properties are different. The data indicate that it represents a new member in the large superfamily of chs and chs-related genes.

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References

  1. Asen S: High pressure liquid chromatographic analysis of flavonoid chemical markers in petals from Gerbera flowers as an adjunct for cultivar and germplasm identification. Phytochemistry 23: 2523–2526 (1984).

    Google Scholar 

  2. Batschauer A, Ehmann B, Schäfer E: Cloning and characterization of a chalcone synthase gene from mustard and its light-dependent expression. Plant Mol Biol 16: 175–185 (1991).

    Google Scholar 

  3. Baumert A, Maier W, Groeger D, Deutzmann R: Purification and properties of acridone synthase from cell suspension cultures of Ruta graveolens. Z Naturforsch 49c: 26–32 (1994).

    Google Scholar 

  4. Bohlmann F, Grenz M: Über die Inhaltsstoffe von Gerbera piloselloides Cass. Chem Ber 108: 26–30 (1975).

    Google Scholar 

  5. Borejsza-Wysocki W, Hrazdina G: Biosynthesis of p-hydroxyphenylbutan-2-one in raspberry fruits and tissue cultures. Phytochemistry 35: 623–628 (1994).

    Google Scholar 

  6. Bowers WS, Ohta T, Cleere JS, Marsella PA: Discovery of insect anti-juvenile hormones in plants. Science 193: 542–547 (1976).

    Google Scholar 

  7. Coe EH, McCormick S, Modena SA: White pollen in maize. J Hered 72: 318–320 (1981).

    Google Scholar 

  8. Coen E, Meyerowitz EMM: The war of whorls: genetic interactions controlling flower development. Nature 353: 31–37 (1991).

    Google Scholar 

  9. Cox KH, Goldberg RB: Analysis of plant gene expression. In: Shaw CH (ed) Plant Molecular Biology: A Practical Approach, pp. 1–34. IRL Press, Oxford (1988).

    Google Scholar 

  10. Dangl JL, Hahlbrock K, Schell J: Regulation and structure of chalcone synthase genes. In: Vasil IK, Schell J (eds) Cell Culture and Somatic Cell Genetics of Plants 4, pp. 155–173. Academic Press, New York (1989).

    Google Scholar 

  11. Davies KM, Bradley JM, Schwinn KE, Markham KR, Podivinsky E: Flavonoid biosynthesis in flower petals of five lines of lisianthus (Eustoma grandiflorum Grise.). Plant Sci 95: 67–77 (1993).

    Google Scholar 

  12. Dellaporta SL, Wood J, Hicks JB: A plant DNA mini-preparation: Version II. Plant Mol Biol Rep 1: 19–21 (1983).

    Google Scholar 

  13. Ehmann B, Schäfer E: Nucleotide sequences encoding two different chalcone synthases expressed in cotyledons of SAN 9789 treated mustard (Sinapis alba L.). Plant Mol Biol 11: 869–870 (1988).

    Google Scholar 

  14. Elomaa P, Honkanen J, Puska R, Seppänen P, Helariutta Y, Mehto M, Kotilainen M, Nevalainen L, Teeri TH: Agrobacterium-mediated transfer of antisense chalcone synthase cDNA to Gerbera hybrida inhibits flower pigmentation. Bio/technology 11: 508–511 (1993).

    Google Scholar 

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

    Google Scholar 

  16. Fliegmann J, Schröder G, Schanz S, Britsch L, Schröder J: Molecular analysis of chalcone and dihydropinosylvin synthase from Scots pine (Pinus sylvestris), and differential regulation of these and related activities in stressed plants. Plant Mol Biol 18: 489–503 (1992).

    Google Scholar 

  17. Franken P, Niesbach-Klösgen U, Weydemann U, Marechal-Drouard L, Saedler H, Wienand U: The duplicated c chalcone synthase genes C2 and Whp (white pollen) of Zea mays are independently regulated; evidence for translational control of Whp expression by the anthocyanin intensifying gene in. EMBO J 10: 2605–2612 (1991).

    Google Scholar 

  18. Gerats AGM, De Vlaming P, Doodeman M, Al B, Schram AW: Genetic control of the conversion of dihydroflavonols into flavonols and anthocyanins in flowers of Petunia hybrida. Planta 155: 364–368 (1982).

    Google Scholar 

  19. Hanahan D: Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580 (1983).

    Google Scholar 

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

    Google Scholar 

  21. Helariutta Y, Elomaa P, Kotilainen M, Seppänen P, Teeri TH: 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 (1993).

    Google Scholar 

  22. Hrazdina G, Kreuzaler F, Hahlbrock K, Grisebach H: Substrate specificity of flavanone synthase from cell suspension culture of parsley and structure of release products in vitro. Arch Biochem Biophys 169: 84–90 (1976).

    Google Scholar 

  23. Jackson D, Roberts K, Martin C: Temporal and spatial control of expression of anthocyanin biosynthetic genes in developing flowers of Antirrhinum majus. Plant J 2: 425–434 (1992).

    Google Scholar 

  24. Jones JDG, Duinsmuir P, Bedbrook J: High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J 4: 2411–2418 (1985).

    Google Scholar 

  25. Koes RE, Spelt CE, Mol JNM: The chalcone synthase multigene family of Petunia hybrida (V30): differential, light-regulated expression during flower development and UV light induction. Plant Mol Biol 12: 213–225 (1989).

    Google Scholar 

  26. Koes RE, Spelt CE, van den Elzen PJM, Mol JNM: Cloning and molecular characterization of the chalcone synthase multigene family of Petunia hybrida. Gene 81: 245–257 (1989).

    Google Scholar 

  27. Koes RE, van Blokland R, Quattrocchio F, van Tunen AJ, Mol JNM: Chalcone synthase promoters in petunia are active in pigmented and unpigmented cell types. Plant Cell 2: 379–392 (1990).

    Google Scholar 

  28. Koes RE, Quattrocchio F, Mol JNM: The flavonoid biosynthetic pathway in plants: function and evolution. Bioessays 16: 123–132 (1994).

    Google Scholar 

  29. Kreuzaler F, Hahlbrock K: Enzymatic synthesis of aromatic compounds in higher plants. Formation of bis-noryangonin (4-hydroxy-6[4-hydroxystyryl]2-pyrone) from p-coumaroyl-CoA and malonyl-CoA. Arch Biochem Biophys 169: 84–90 (1975).

    Google Scholar 

  30. Lanz T, Tropf S, Marner F-J, Schröder J, Schröder G: The role of cysteines in polyketide synthases: site-directed mutagenesis of resveratrol and chalcone synthases, two key enzymes in different plant-specific pathways. J Biol Chem 266: 9971–9976 (1991).

    Google Scholar 

  31. Martin C, Carpenter R, Coen ES, Gerats AGM: The control of floral pigmentation in Antirrhinum majus. In: Thomas H, Grierson D (eds) Developmental Mutations in Plants (SEB Seminar Series 32), pp. 19–53. Cambridge University Press, Cambridge (1987).

    Google Scholar 

  32. Martin C, Gerats T: Control of pigment biosynthesis genes during petal development. Plant Cell 5: 1253–1264 (1993).

    Google Scholar 

  33. Melchior F, Kindl H: Grapevine stilbene synthase cDNA only slightly differing from chalcone synthase cDNA is expressed in Escherichia coli into catalytically active enzyme. FEBS Lett 268: 17–20 (1990).

    Google Scholar 

  34. Nakajima O, Akiyama T, Hakamatsuka T, Shibuya M, Noguchi H, Ebizuka Y, Sankawa U: Isolation, sequencing and bacterial expression of a cDNA for chalcone synthase from the cultured cells of Pueraria lobata. Chem Pharm Bull 39: 1911–1913 (1991).

    Google Scholar 

  35. Niesbach-Klösgen U, Barzen E, Bernhardt J, Rohde W, Schwarz-Sommer Z, Reif HJ, Wienand U, Saedler H: Chalcone synthase genes in plants: a tool to study evolutionary relationships. J Mol Evol 26: 213–225 (1987).

    Google Scholar 

  36. Ohl S, Hahlbrock K, Schäfer E: A stable blue-light-derived signal modulates ultraviolet-light-induced activation of the chalcone-synthase gene in cultured parsley cells. Planta 177: 228–236 (1989).

    Google Scholar 

  37. Proksch P, Rodriquez E: Chromenes and benzofurans of the Asteraceae. Their chemistry and biological significance. Phytochemistry 22: 2335–2348 (1983).

    Google Scholar 

  38. Quattrocchio F, Wing JF, Leppen HTC, Mol JNM, Koes RE: Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5: 1497–1512 (1993).

    Google Scholar 

  39. Recourt K, van Tunen AJ, Mur L, van Brussel AAN, Lugtenberg BJJ, Kijne JW: Activation of flavonoid biosynthesis in roots of Vicia sativa subsp. nigra plants by inoculation with Rhizobium leguminosarum biovar viciae. Plant Mol Biol 19: 411–420 (1992).

    Google Scholar 

  40. Reimold U, Kroeger M, Kreuzaler F, Hahlbrock K: Coding and 3′ non-coding nucleotide sequence of chalcone synthase mRNA and assignment of amino acid sequence of the enzyme. EMBO J 2: 1801–1805 (1983).

    Google Scholar 

  41. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York (1989).

    Google Scholar 

  42. Sancar A, Hack AM, Rupp WD: Simple method for identification of plasmid-coded proteins. J Bact 137: 692–693 (1979).

    Google Scholar 

  43. Schanz S, Schröder G, Schröder J: Stilbene synthase from Scots pine (Pinus sylvestris). FEBS Lett 313: 71–74 (1992).

    Google Scholar 

  44. Schmid J, Doerner PW, Clouse SD, Dixon RA, Lamb CJ: Developmental and environmental regulation of a bean chalcone synthase promoter in transgenic tobacco. Plant Cell 2: 619–631 (1990).

    Google Scholar 

  45. Schröder G, Brown JWS, Schröder J: Molecular analysis of resveratrol synthase: cDNA, genomic clones and relationship with chalcone synthase. Eur J Biochem 172: 161–169 (1988).

    Google Scholar 

  46. Schröder J, Schröder G: Stilbene and chalcone synthases: related enzymes with key functions in plant specific pathways. Z Naturforsch 45c: 1–8 (1990).

    Google Scholar 

  47. Schüz R, Heller W, Hahlbrock K: Substrate specificity of chalcone synthase from Petroselinum hortense. J Biol Chem 258: 6730–6734 (1983).

    Google Scholar 

  48. Shen JB, Hsu F: Brassica anther-specific genes: characterization and in situ localization of expression. Mol Gen Genet 234: 379–389 (1992).

    Google Scholar 

  49. Siebertz R, Proksch P, Witte L: Accumulation and biosynthesis of the chromenes precocene I and II in Ageratum houstonianum. Phytochemistry 29: 2135–2138 (1990).

    Google Scholar 

  50. Sommer H, Saedler H: Structure of the chalcone synthase gene of Antirrhinum majus. Mol Gen Genet 202: 429–434 (1986).

    Google Scholar 

  51. Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C: Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24: 743–755 (1994).

    Google Scholar 

  52. Stich K, Eidenberger T, Wurst F, Forkmann G: Flavonol synthase activity and regulation of flavonol and anthocyanin biosynthesis during flower development in Dianthus caryophyllus L. (carnation). Z Naturforsch 47c: 553–560 (1992).

    Google Scholar 

  53. Takkinen K, Laukkanen M-L, Sizmann D, Alfthan K, Immonen T, Vanne L, Kaartinen M, Knowles JKC, Teeri TT: An active single-chain antibody containing a cellulase linker domain is secreted by Escherichia coli. Protein Eng 4: 837–841 (1991).

    Google Scholar 

  54. Taylor LP, Briggs W: Genetic regulation and photocontrol of anthocyanin accumulation in maize seedlings. Plant Cell 2: 115–128 (1990).

    Google Scholar 

  55. Taylor LP, Jorgensen R: Conditional male fertility in chalcone synthase-deficient petunia. J Hered 83: 11–17 (1992).

    Google Scholar 

  56. Tropf S, Lanz T, Rensing SA, Schröder J, Schröder G: Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. J Mol Evol 38: 610–618 (1994).

    Google Scholar 

  57. van Brussel AAN, Recourt K, Pees E, Spaink HP, Teun T, Wijffelman CA, Kijne JW, Lugtenberg BJJ: A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. J Bact 172: 5394–5401 (1990).

    Google Scholar 

  58. van der Meer IM, Stam ME, van Tunen AJ, Mol JNM, Stuije AR: Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4: 253–262 (1992).

    Google Scholar 

  59. Weiss D, van der Huit AH, Kroon JTM, Mol JNM, Kooter JM: The Petunia homologue of the Antirrhinum candi and Zea mays A2 flavonoid genes; homology to flavanone 3-hydroxylase and ethylene forming enzyme. Plant Mol Biol 22: 893–897 (1993).

    Google Scholar 

  60. Wienand U, Weydemann U, Niesbach-Klösgen U, Peterson PA, Saedler H: Molecular cloning of the c2 locus of Zea mays the gene coding for chalcone synthase. Mol Gen Genet 203: 202–207 (1986).

    Google Scholar 

  61. Wingender R, Röhrig H, Höriche C, Wing D, Schell J: Differential regulation of soybean chalcone synthase genes in plant defense, symbiosis and upon environmental stimuli. Mol Gen Genet 218: 315–322 (1989).

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biotechnology, University of Helsinki, P.O. Box 45, FIN-00014, Helsinki, Finland

    Yrjö Helariutta, Paula Elomaa, Mika Kotilainen & Teemu H. Teeri

  2. Floral/Nursery Plants Research, U.S. National Arboretum, U.S. Department of Agriculture, 20705-2350, Beltsville, MD, USA

    Robert J. Griesbach

  3. Institut für Biologie II, Biochemie der Pflanzen, Universität Freiburg, Schänzlestrasse 1, D-79104, Freiburg, Germany

    Joachim Schröder

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  1. Yrjö Helariutta
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Helariutta, Y., Elomaa, P., Kotilainen, M. et al. Chalcone synthase-like genes active during corolla development are differentially expressed and encode enzymes with different catalytic properties in Gerbera hybrida (Asteraceae). Plant Mol Biol 28, 47–60 (1995). https://doi.org/10.1007/BF00042037

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