Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Aug 20;93(17):9033–9038. doi: 10.1073/pnas.93.17.9033

Duplication and functional divergence in the chalcone synthase gene family of Asteraceae: evolution with substrate change and catalytic simplification.

Y Helariutta 1, M Kotilainen 1, P Elomaa 1, N Kalkkinen 1, K Bremer 1, T H Teeri 1, V A Albert 1
PMCID: PMC38590  PMID: 8799149

Abstract

Plant-specific polyketide synthase genes constitute a gene superfamily, including universal chalcone synthase [CHS; malonyl-CoA:4-coumaroyl-CoA malonyltransferase (cyclizing) (EC 2.3.1.74)] genes, sporadically distributed stilbene synthase (SS) genes, and atypical, as-yet-uncharacterized CHS-like genes. We have recently isolated from Gerbera hybrida (Asteraceae) an unusual CHS-like gene, GCHS2, which codes for an enzyme with structural and enzymatic properties as well as ontogenetic distribution distinct from both CHS and SS. Here, we show that the GCHS2-like function is encoded in the Gerbera genome by a family of at least three transcriptionally active genes. Conservation within the GCHS2 family was exploited with selective PCR to study the occurrence of GCHS2-like genes in other Asteraceae. Parsimony analysis of the amplified sequences together with CHS-like genes isolated from other taxa of angiosperm subclass Asteridae suggests that GCHS2 has evolved from CHS via a gene duplication event that occurred before the diversification of the Asteraceae. Enzyme activity analysis of proteins produced in vitro indicates that the GCHS2 reaction is a non-SS variant of the CHS reaction, with both different substrate specificity (to benzoyl-CoA) and a truncated catalytic profile. Together with the recent results of Durbin et al. [Durbin, M. L., Learn, G. H., Jr., Huttley, G. A. & Clegg, M. T. (1995) Proc. Natl. Acad. Sci. USA 92, 3338-3342], our study confirms a gene duplication-based model that explains how various related functions have arisen from CHS during plant evolution.

Full text

PDF
9033

Images in this article

9037Fig. 3
on p.9037

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baumert A., Maier W., Gröger D., Deutzmann R. Purification and properties of acridone synthase from cell suspension cultures of Ruta graveolens L. Z Naturforsch C. 1994 Jan-Feb;49(1-2):26–32. doi: 10.1515/znc-1994-1-205. [DOI] [PubMed] [Google Scholar]
  2. Courtney-Gutterson N., Napoli C., Lemieux C., Morgan A., Firoozabady E., Robinson K. E. Modification of flower color in florist's chrysanthemum: production of a white-flowering variety through molecular genetics. Biotechnology (N Y) 1994 Mar;12(3):268–271. doi: 10.1038/nbt0394-268. [DOI] [PubMed] [Google Scholar]
  3. Durbin M. L., Learn G. H., Jr, Huttley G. A., Clegg M. T. Evolution of the chalcone synthase gene family in the genus Ipomoea. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3338–3342. doi: 10.1073/pnas.92.8.3338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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 enzyme activities in stressed plants. Plant Mol Biol. 1992 Feb;18(3):489–503. doi: 10.1007/BF00040665. [DOI] [PubMed] [Google Scholar]
  5. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  6. Helariutta Y., Elomaa P., Kotilainen M., Griesbach R. J., Schröder J., Teeri T. H. 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. 1995 Apr;28(1):47–60. doi: 10.1007/BF00042037. [DOI] [PubMed] [Google Scholar]
  7. Junghanns K. T., Kneusel R. E., Baumert A., Maier W., Gröger D., Matern U. Molecular cloning and heterologous expression of acridone synthase from elicited Ruta graveolens L. cell suspension cultures. Plant Mol Biol. 1995 Feb;27(4):681–692. doi: 10.1007/BF00020222. [DOI] [PubMed] [Google Scholar]
  8. Kauppinen S., Siggaard-Andersen M., von Wettstein-Knowles P. beta-Ketoacyl-ACP synthase I of Escherichia coli: nucleotide sequence of the fabB gene and identification of the cerulenin binding residue. Carlsberg Res Commun. 1988;53(6):357–370. doi: 10.1007/BF02983311. [DOI] [PubMed] [Google Scholar]
  9. Koes R. E., Spelt C. E., van den Elzen P. J., Mol J. N. Cloning and molecular characterization of the chalcone synthase multigene family of Petunia hybrida. Gene. 1989 Sep 30;81(2):245–257. doi: 10.1016/0378-1119(89)90185-6. [DOI] [PubMed] [Google Scholar]
  10. 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. 1975 Jul;169(1):84–90. doi: 10.1016/0003-9861(75)90319-7. [DOI] [PubMed] [Google Scholar]
  11. Melchior F., Kindl H. Grapevine stilbene synthase cDNA only slightly differing from chalcone synthase cDNA is expressed in Escherichia coli into a catalytically active enzyme. FEBS Lett. 1990 Jul 30;268(1):17–20. doi: 10.1016/0014-5793(90)80961-h. [DOI] [PubMed] [Google Scholar]
  12. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  13. Schröder G., Brown J. W., Schröder J. Molecular analysis of resveratrol synthase. cDNA, genomic clones and relationship with chalcone synthase. Eur J Biochem. 1988 Feb 15;172(1):161–169. doi: 10.1111/j.1432-1033.1988.tb13868.x. [DOI] [PubMed] [Google Scholar]
  14. Schüz R., Heller W., Hahlbrock K. Substrate specificity of chalcone synthase from Petroselinum hortense. Formation of phloroglucinol derivatives from aliphatic substrates. J Biol Chem. 1983 Jun 10;258(11):6730–6734. [PubMed] [Google Scholar]
  15. Shen J. B., Hsu F. C. Brassica anther-specific genes: characterization and in situ localization of expression. Mol Gen Genet. 1992 Sep;234(3):379–389. doi: 10.1007/BF00538697. [DOI] [PubMed] [Google Scholar]
  16. 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. 1994 Mar;24(5):743–755. doi: 10.1007/BF00029856. [DOI] [PubMed] [Google Scholar]
  17. Stafford H. A. Flavonoid evolution: an enzymic approach. Plant Physiol. 1991 Jul;96(3):680–685. doi: 10.1104/pp.96.3.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Takkinen K., Laukkanen M. L., Sizmann D., Alfthan K., Immonen T., Vanne L., Kaartinen M., Knowles J. K., Teeri T. T. An active single-chain antibody containing a cellulase linker domain is secreted by Escherichia coli. Protein Eng. 1991 Oct;4(7):837–841. doi: 10.1093/protein/4.7.837. [DOI] [PubMed] [Google Scholar]
  19. Tropf S., Lanz T., Rensing S. A., Schröder J., Schröder G. Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. J Mol Evol. 1994 Jun;38(6):610–618. doi: 10.1007/BF00175881. [DOI] [PubMed] [Google Scholar]
  20. Verwoert I. I., Verbree E. C., van der Linden K. H., Nijkamp H. J., Stuitje A. R. Cloning, nucleotide sequence, and expression of the Escherichia coli fabD gene, encoding malonyl coenzyme A-acyl carrier protein transacylase. J Bacteriol. 1992 May;174(9):2851–2857. doi: 10.1128/jb.174.9.2851-2857.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Vieira J., Messing J. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene. 1991 Apr;100:189–194. doi: 10.1016/0378-1119(91)90365-i. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES