Abstract
Chalcone synthase (CHS) is a key enzyme in the biosynthesis of flavonoides, which are important for the pigmentation of flowers and act as attractants to pollinators. Genes encoding CHS constitute a multigene family in which the copy number varies among plant species and functional divergence appears to have occurred repeatedly. In morning glories (Ipomoea), five functional CHS genes (A–E) have been described. Phylogenetic analysis of the Ipomoea CHS gene family revealed that CHS A, B, and C experienced accelerated rates of amino acid substitution relative to CHS D and E. To examine whether the CHS genes of the morning glories underwent adaptive evolution, maximum-likelihood models of codon substitution were used to analyze the functional sequences in the Ipomoea CHS gene family. These models used the nonsynonymous/synonymous rate ratio (ω = d N /d S ) as an indicator of selective pressure and allowed the ratio to vary among lineages or sites. Likelihood ratio test suggested significant variation in selection pressure among amino acid sites, with a small proportion of them detected to be under positive selection along the branches ancestral to CHS A, B, and C. Positive Darwinian selection appears to have promoted the divergence of subfamily ABC and subfamily DE and is at least partially responsible for a rate increase following gene duplication.
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References
JP Bielawski Z Yang (2001) ArticleTitlePositive and negative selection in the DAZ gene family. Mol Biol Evol 18 523–529 Occurrence Handle1:CAS:528:DC%2BD3MXis1eisLk%3D Occurrence Handle11264403
MT Clegg ML Durbin (2000) ArticleTitleFlower color variation: A model for the experimental study of evolution. Proc Natl Acad Sci USA 97 7016–7023 Occurrence Handle10.1073/pnas.97.13.7016 Occurrence Handle1:CAS:528:DC%2BD3cXksVKisb0%3D Occurrence Handle10860965
MT Clegg ML Durbin (2003) ArticleTitleTracing floral adaptations from ecology to molecules. Nature Rev Genet 4 260–215
PM Debnam G Shearer L Blackwood DH Kohl (1997) ArticleTitleEvidence for channeling of intermediates in the oxidative pentose phosphate pathway by soybean and pea nodule extracts, yeast extracts, and purified yeast enzymes. Eur J Biochem 246 283–290 Occurrence Handle1:CAS:528:DyaK2sXjvVGrtrk%3D Occurrence Handle9208916
ML Durbin GH Learn GA Huttley MT Clegg (1995) ArticleTitleEvolution of the chalcone synthase gene family in the genus Ipomoea. Proc Natl Acad Sci USA 92 3338–3342 Occurrence Handle1:CAS:528:DyaK2MXltFSntbc%3D Occurrence Handle7724563
ML Durbin B McCaig MT Clegg (2000) ArticleTitleMolecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol Biol 42 79–92 Occurrence Handle10.1023/A:1006375904820 Occurrence Handle1:CAS:528:DC%2BD3cXht1Gku7c%3D Occurrence Handle10688131
S Eckermann G Schröder J Schmidt D Strack RA Edrada Y Helariutta P Elomaa I Kotilainen P Proksch TH Teeri J Schröder (1998) ArticleTitleNew pathway to polyketides in plants. Nature 396 390–397 Occurrence Handle10.1038/24652 Occurrence Handle9845078
JL Ferrer JM Jez ME Bowman RA Dixon JP Noel (1999) ArticleTitleStructure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nature Struct Biol 6 775–784 Occurrence Handle10.1038/11553 Occurrence Handle1:CAS:528:DyaK1MXltVShsLg%3D
S Fukada-Tanaka A Hoshino Y Hisatomi Y Habu M Hasebe S Iida (1997) ArticleTitleIdentification of new chalcone synthase genes for flower pigmentation in the Japanese and common morning glories. Plant Cell Physiol 38 754–758 Occurrence Handle1:CAS:528:DyaK2sXktVKkur4%3D Occurrence Handle9249990
N Goldman Z Yang (1994) ArticleTitleA codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11 725–736 Occurrence Handle7968486
M Hasegawa H Kishino T Yano (1985) ArticleTitleDating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22 160–174 Occurrence Handle1:CAS:528:DyaL2MXmtFSns7g%3D Occurrence Handle3934395
Y Helariutta M Kotilainen P Elomaa N Kalkkinen K Bremer TH Teeri VA Albert (1996) ArticleTitleDuplication and functional divergence in the chalcone synthase gene family of Asteraceae: Evolution with substrate change and catalytic simplification. Proc Natl Acad Sci USA 93 9033–9038 Occurrence Handle10.1073/pnas.93.17.9033 Occurrence Handle1:CAS:528:DyaK28Xlt1Chsrw%3D Occurrence Handle8799149
G Hrazdina RA Jensen (1992) ArticleTitleSpatial organization of enzymes in plant metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 43 241–267 Occurrence Handle10.1146/annurev.pp.43.060192.001325 Occurrence Handle1:CAS:528:DyaK38Xks1Knur0%3D
JP Huelsenbeck F Ronquist (2001) ArticleTitleMrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17 754–755 Occurrence Handle10.1093/bioinformatics/17.8.754 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D Occurrence Handle11524383
JM Jez MB Austin JL Ferrer ME Bowman J Schröder JP Noel (2000) ArticleTitleStructural control of polyketide formation in plant-specific polyketide synthases. Chem Biol 7 919–930 Occurrence Handle1:CAS:528:DC%2BD3MXltFegtg%3D%3D Occurrence Handle11137815
JM Jez ME Bowman JP Noel (2001) ArticleTitleStructure-guided programming of polyketide chain-length determination in chalcone synthase. Biochemistry 40 14829–14838 Occurrence Handle10.1021/bi015621z Occurrence Handle1:CAS:528:DC%2BD3MXotFyrsrY%3D Occurrence Handle11732902
M Kimura (1983) The neutral theory of molecular evolution. Cambridge University Press Cambridge, UK
RE Koes CE Spelt JNM Mol AG Gerats (1987) ArticleTitleThe chalcone synthase multigene family of Petunia hybrida (V30): Sequence homology, chromosomal localization and evolutionary aspects. Plant Mol Biol 10 159–169 Occurrence Handle1:CAS:528:DyaL1cXovVymuw%3D%3D
RE Koes CE Spelt PJM van den Elzen JNM Mol (1989) ArticleTitleCloning and molecular characterization of the chalcone synthase multigene family of Petunia hybrida. Gene 81 245–257 Occurrence Handle10.1016/0378-1119(89)90185-6 Occurrence Handle1:CAS:528:DyaK3cXitFWksLc%3D Occurrence Handle2806915
W-H Li (1985) Accelerated evolution following gene duplication and its implications for the neutralist-selectionist controversy. T Otha K Aoki (Eds) Population genetics and molecular evolution. Japan Scientific Press, Tokyo 333–352
W-H Li (1997) Molecular evolution. Sinauer Sunderland, MA
R Lukacin K Springob C Urbanke C Ernwein G Schröder J Schröder U Matern (1999) ArticleTitleNative acridone synthase I and II from Ruta graveolens L. form homodimers. FEBS Lett 448 135–140 Occurrence Handle10.1016/S0014-5793(99)00355-5 Occurrence Handle1:CAS:528:DyaK1MXit1Wrtbw%3D Occurrence Handle10217426
SV Muse BS Gaut (1994) ArticleTitleA likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates with application to the chloroplast genome. Mol Bio Evol 11 715–724 Occurrence Handle1:CAS:528:DyaK2cXlvFOjsL8%3D
R Nielsen Z Yang (1998) ArticleTitleLikelihood models for detecting positively selected amino acid sites and application to the HIV-1 envelop gene. Genetics 148 929–936 Occurrence Handle1:CAS:528:DyaK1cXks1eitr8%3D Occurrence Handle9539414
S Ohno (1970) Evolution by gene duplication. Springer-Verlag New York
T Ohta (1993) ArticleTitlePattern of nucleotide substitution in growth hormone-prolactin gene family: A paradigm for evolution by gene duplication. Genetics 134 1271–1276 Occurrence Handle1:CAS:528:DyaK2cXht1KltLs%3D Occurrence Handle8375661
NB Paniego KWM Zuurbier SY Fung R Van der Heijden JJC Scheffer R Verpoorte (1999) ArticleTitlePhlorisovalerophenone synthase, a novel polyketide synthase from hop (Humulus lupulus L.) cones. Eur J Biochem 262 612–616 Occurrence Handle10.1046/j.1432-1327.1999.00444.x Occurrence Handle1:CAS:528:DyaK1MXjvVGmtLg%3D Occurrence Handle10336650
SK Pond (2001) Hypothesis testing using phylogenies (HYPHY), version 0.91 beta. University of Arizona Tucson
R Preisig-Müller P Gnau H Kindl (1995) ArticleTitleThe inducible 9,10-dihydrophenanthrene pathway: Characterization and expression of bibenzyl synthase and S-adenosylhomocysteine hydrolase. Arch Biochem Biophys 317 201–207 Occurrence Handle10.1006/abbi.1995.1154 Occurrence Handle7872785
B Rannala Z Yang (1996) ArticleTitleProbability distribution of molecular evolutionary trees: A new method of phylogenetic inference. J Mol Evol 43 304–311 Occurrence Handle1:CAS:528:DyaK28XlvVahur8%3D Occurrence Handle8703097
N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015
A Schöppner H Kindl (1984) ArticleTitlePurification and properties of a stilbene synthase from induced cell suspension cultures of peanut. J Biol Chem 259 6806–6811 Occurrence Handle1:CAS:528:DyaL2cXkvVKit7g%3D Occurrence Handle6427224
J Schröder (1997) ArticleTitleA family of plant-specific polyketide synthases: Facts and predictions. Trends Plant Sci 2 373–378 Occurrence Handle10.1016/S1360-1385(97)01104-7
PA Srere B Sumegi AD Sherry (1987) ArticleTitleOrganizational aspects of the citric acid cycle. Biochem Soc Symp 54 173–182 Occurrence Handle1:CAS:528:DyaL1cXmt1Cru74%3D Occurrence Handle3332994
DK Srivastava SA Bernhard (1986) ArticleTitleMetabolite transfer via enzyme-enzyme complexes. Science 234 1081–1084 Occurrence Handle1:CAS:528:DyaL2sXotVCitw%3D%3D Occurrence Handle3775377
HA Stafford (1991) ArticleTitleFlavonoid evolution: An enzymic approach. Plant Physiol 96 680–685 Occurrence Handle1:CAS:528:DyaK3MXltFSmsbc%3D
DL Swofford (1998) PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0. Sunderland, MA
JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 4876–4882 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791
S Tropf T Lanz SA Rensing J Schröder G Schröder (1994) ArticleTitleEvidence that stibene synthases have developed from chalcone synthases several times in the course of evolution. J Mol Evol 38 610–618 Occurrence Handle1:CAS:528:DyaK2cXkt12rt70%3D Occurrence Handle8083886
JB Walsh (1995) ArticleTitleHow often do duplicated genes evolve new functions? Genetics 139 421–428 Occurrence Handle1:STN:280:ByqB38%2FmvVQ%3D Occurrence Handle7705642
J Yang J Huang H Gu Y Zhong Z Yang (2002) ArticleTitleDuplication and adaptive evolution of the chalcone synthase genes of Dendranthema (Asteraceae). Mol Biol Evol 19 1752–1759 Occurrence Handle1:CAS:528:DC%2BD38XnvFSlu7w%3D Occurrence Handle12270901
Z Yang (1994) ArticleTitleMaximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39 306–314 Occurrence Handle7932792
Z Yang (1997) ArticleTitlePAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555–556 Occurrence Handle9367129
Z Yang (1998) ArticleTitleLikelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15 568–573 Occurrence Handle9580986
Z Yang JP Bielawski (2000) ArticleTitleStatistical methods for detecting molecular adaptation. Trends Ecol Evol 15 496–503 Occurrence Handle10.1016/S0169-5347(00)01994-7 Occurrence Handle11114436
Z Yang R Nielsen (1998) ArticleTitleSynonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46 409–418 Occurrence Handle1:CAS:528:DyaK1cXitlSgu7w%3D Occurrence Handle9541535
Z Yang R Nielsen (2000) ArticleTitleEstimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17 32–43 Occurrence Handle1:CAS:528:DC%2BD3cXotF2qtA%3D%3D Occurrence Handle10666704
Z Yang R Nielsen (2002) ArticleTitleCodon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19 908–917 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtbk%3D Occurrence Handle12032247
Z Yang R Nielsen N Goldman AMK Pedersen (2000) ArticleTitleCodon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155 431–449
Acknowledgements
We thank two anonymous reviewers for comments. This study was supported by National Natural Science Foundation of China Grant 39830020 to H.G., and HFSP Grant Y0055/2001-M and BBSRC Grant 31/G14969 to Z.Y.
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Yang, J., Gu, H. & Yang, Z. Likelihood Analysis of the Chalcone Synthase Genes Suggests the Role of Positive Selection in Morning Glories (Ipomoea) . J Mol Evol 58, 54–63 (2004). https://doi.org/10.1007/s00239-003-2525-3
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DOI: https://doi.org/10.1007/s00239-003-2525-3