Abstract
Enzymes of the chalcone synthase (CHS) superfamily catalyze the production of a variety of secondary metabolites in bacteria, fungi and plants. Some of these metabolites have played important roles during the early evolution of land plants by providing protection from various environmental assaults including UV irradiation. The genome of the moss, Physcomitrella patens, contains at least 17 putative CHS superfamily genes. Three of these genes (PpCHS2b, PpCHS3 and PpCHS5) exist in multiple copies and all have corresponding ESTs. PpCHS11 and probably also PpCHS9 encode non-CHS enzymes, while PpCHS10 appears to be an ortholog of plant genes encoding anther-specific CHS-like enzymes. It was inferred from the genomic locations of genes comprising it that the moss CHS superfamily expanded through tandem and segmental duplication events. Inferred exon–intron architectures and results from phylogenetic analysis of representative CHS superfamily genes of P. patens and other plants showed that intron gain and loss occurred several times during evolution of this gene superfamily. A high proportion of P. patens CHS genes (7 of 14 genes for which the full sequence is known and probably 3 additional genes) are intronless, prompting speculation that CHS gene duplication via retrotransposition has occurred at least twice in the moss lineage. Analyses of sequence similarities, catalytic motifs and EST data indicated that a surprisingly large number (as many as 13) of the moss CHS superfamily genes probably encode active CHS. EST distribution data and different light responsiveness observed with selected genes provide evidence for their differential regulation. Observed diversity within the moss CHS superfamily and amenability to gene manipulation make Physcomitrella a highly suitable model system for studying expansion and functional diversification of the plant CHS superfamily of genes.
Similar content being viewed by others
References
Abe I, Sano Y, Takahashi Y, Noguchi H (2003) Site-directed mutagenesis of benzalacetone synthase. The role of the Phe215 in plant type III polyketide synthases. J Biol Chem 278:25218–25226
Abe I, Oguro S, Utsumi Y, Sano Y, Noguchi H (2005) Engineered biosynthesis of plant polyketides: chain length control in an octaketide-producing plant type III polyketide synthase. J Am Chem Soc 127:12709–12716
Ageez A, Kazama Y, Sugiyama R, Kawano S (2005) Male-fertility genes expressed in male flower buds of Silene latifolia include homologs of anther-specific genes. Genes Genet Syst 80:403–413
Akiyama T, Shibuya M, Liu HM, Ebizuka Y (1999) p-Coumaroyltriacetic acid synthase, a new homologue of chalcone synthase, from Hydrangea macrophylla var. thunbergii. Eur J Biochem 263:834–839
Ashton NW, Schulze A, Hall P, Bandurski RS (1985) Estimation of indole-3-acetic acid in gametophytes of the moss, Physcomitrella patens. Planta 164:142–144
Atanassov I, Russinova E, Antonov L, Atanassov A (1998) Expression of an anther-specific chalcone synthase-like gene is correlated with uninucleate microspore development in Nicotiana sylvestris. Plant Mol Biol 38:1169–1178
Austin MB, Noel JP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20:79–110
Austin MB, Bowman ME, Ferrer JL, Schroder J, Noel JP (2004) An aldol switch discovered in stilbene synthases mediates cyclization specificity of type III polyketide synthases. Chem Biol 11:1179–1194
Basile A, Sorbo S, Lopez-Saez JA, Cobianchi RC (2003) Effects of seven pure flavonoids from mosses on germination and growth of Tortula muralis HEDW (Bryophyta) and Raphanus sativus L (Magnoliophyta). Phytochemistry 62:1145–1151
Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292
Brinkmeier E, Geiger H, Zinsmeister HD (1999) Biflavonoids and 4, 2′-epoxy-3-phenylcoumarins from the moss Mnium hornum. Phytochemistry 52:297–302
Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165:886–894
Dipp NJ, Newman AJ (1989) Evidence that introns arose at proto-splice site. EMBO J 8:2015–2021
Domínguez E, Mercado JA, Quesada MA, Heredia A (1999) Pollen sporopollenin: degradation and structural elucidation. Sex Plant Reprod 12:171–178
Durbin ML, McCaig B, Clegg MT (2000) Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol Biol 42:79–92
Eckermann S, Schröder G, Schmidt J, Strack D, Edrada RA, Helariutta Y, Elomaa P, Kotilainen M, Kilpeläinen I, Proksch P, Teeri TH, Schröder J (1998) New pathway to polyketides in plants. Nature 396:387–390
Ferrer JL, Jez JM, Bowman ME, Dixon RA, Noel JP (1999) Structure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nat Struct Biol 6:775–784
Fliegmann J, Schröder G, Schanz S, Britsch L, Schröder J (1992) 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 18:489–503
Frugoli JA, McPeek MA, Thomas TL, McClung CR (1998) Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics 149:355–365
Fujita Y (1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol 37:411–421
Fukuma K, Neuls ED, Ryberg JM, Suh D-Y, Sankawa U (2007) Mutational analysis of conserved outer sphere arginine residues of chalcone synthase. J Biochem 142:731–739
Funa N, Ozawa H, Hirata A, Horinouchi S (2006) Phenolic lipid synthesis by type III polyketide synthases is essential for cyst formation in Azotobacter vinelandii. Proc Natl Acad Sci USA 103:6356–6361
Funa N, Awakawa T, Horinouchi S (2007) Pentaketide resorcylic acid synthesis by type III polyketide synthase from Neurospora crassa. J Biol Chem 282:14476–14481
Geiger H, Markham KR (1992) Campylopusaurone, an auronoflavanone biflavonoid from the mosses Campylopus clavatus and Campylopus holomitrium. Phytochemistry 31:4325–4328
Gross F, Luniak N, Perlova O, Gaitatzis N, Jenke-Kodama H, Gerth K, Gottschalk D, Dittmann E, Muller R (2006) Bacterial type III polyketide synthases: phylogenetic analysis and potential for the production of novel secondary metabolites by heterologous expression in pseudomonads. Arch Microbiol 185:28–38
Häger KP, Müller B, Wind C, Erbach S, Fischer H (1996) Evolution of legumin genes: loss of an ancestral intron at the beginning of angiosperm diversification. FEBS Lett 387:94–98
Han Y-Y, Ming F, Wang W, Wang J-W, Ye M-M, Shen D-L (2006) Molecular evolution and functional specialization of chalcone synthase superfamily from Phalaenopsis Orchid. Genetica 128:429–438
Harashima S, Takano H, Ono K, Takio S (2004) Chalcone synthase-like gene in the liverwort, Marchantia paleacea var. diptera. Plant Cell Rep 23:167–173
Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57:155–171
Höfig KP, Moyle RL, Putterill J, Walter C (2003) Expression analysis of four Pinus radiata male cone promoters in the heterogeneous host Arabidopsis. Planta 217:858–867
Iwashina T (2000) The structure and distribution of the flavonoids in plants. J Plant Res 113:287–299
Jez JM, Noel JP (2000) Mechanism of chalcone synthase. pKa of the catalytic cysteine and the role of the conserved histidine in a plant polyketide synthase. J Biol Chem 275:39640–39646
Jez JM, Austin MB, Ferrer J, Bowman ME, Schröder J, Noel JP (2000a) Structural control of polyketide formation in plant-specific polyketide synthases. Chem Biol 7:919–930
Jez JM, Ferrer JL, Bowman ME, Dixon RA, Noel JP (2000b) Dissection of malonyl-coenzyme a decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry 39:890–902
Jez JM, Bowman ME, Noel JP (2002) Expanding the biosynthetic repertoire of plant type III polyketide synthases by altering starter molecule specificity. Proc Natl Acad Sci USA 99:5319–5324
Jiang C, Schommer CK, Kim SY, Suh D-Y (2006) Cloning and characterization of chalcone synthase from the moss, Physcomitrella patens. Phytochemistry 67:2531–2540
Jiang C, Kim SY, Suh D-Y (2008) Divergent evolution of the thiolase superfamily and chalcone synthase family. Mol Phylogenet Evol 49:691–701
Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585
Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993–1001
Kamisugi Y, Cuming AC, Cove DJ (2005) Parameters determining the efficiency of gene targeting in the moss Physcomitrella patens. Nucleic Acids Res 33:e173
Kamisugi Y, Schlink K, Rensing SA, Schween G, von Stackelberg M, Cuming AC, Reski R, Cove DJ (2006) The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res 34:6205–6214
Koes RE, Spelt CE, Mol JNM (1989) 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
Kumar S, Tamura K, Nei M (2004) MEGA3: Intergrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Lang D, Eisinger J, Reski R, Rensing S (2005) Representation and high-quality annotation of the Physcomitrella patens transcriptome demonstrates a high proportion of proteins involved in metabolism in mosses. Plant Biol 7:238–250
Lanz T, Tropf S, Marner F-J, Schröder J, Schröder G (1991) 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
Liu B, Falkenstein-Paul H, Schmidt W, Beerhues L (2003) Benzophenone synthase and chalcone synthase from Hypericum androsaemum cell cultures: cDNA cloning, functional expression, and site-directed mutagenesis of two polyketide synthases. Plant J 34:847–855
Liu B, Raeth T, Beuerle T, Beerhues L (2007) Biphenyl synthase, a novel type III polyketide synthase. Planta 225:1495–1503
Loake GJ, Faktor O, Lamb CJ, Dixon RA (1992) Combination of H-box [CCTACC(N)7CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc Natl Acad Sci USA 89:9230–9234
Long M, Rosenberg C (2000) Testing the “proto-splice sites” model of intron origin: evidence from analysis of intron phase correlations. Mol Biol Evol 17:1789–1796
Lütcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA (1987) Selection of AUG codons differs in plants and animals. EMBO J 6:43–48
Ma L-Q, Pang X-B, Shen H-Y, Pu GB, Wang HH, Lei CY, Wang H, Li GF, Liu BY, Ye HC (2009) A novel type III polyketide synthase encoded by a three-intron gene from Polygonum cuspidatum. Planta 229:457–469
Markham KR (1988) Distribution of flavonoids in the lower plants and its evolutionary significance. In: Harborne JB (ed) The flavonoids. Chapman and Hall, London, pp 427–468
Mizuuchi Y, Shimokawa Y, Wanibuchi K, Noguchi H, Abe I (2008) Structure function analysis of novel type III polyketide synthases from Arabidopsis thaliana. Biol Pharm Bull 31:2205–2210
Morita H, Kondo S, Oguro S, Noguchi H, Sugio S, Abe I, Kohno T (2007) Structural insight into chain-length control and product specificity of pentaketide chromone synthase from Aloe arborescens. Chem Biol 14:359–369
Nishiyama T, Fujita T, Shin-I T, Seki M, Nishide H, Uchiyama I, Kamiya A, Carninci P, Hayashizaki Y, Shinozaki K, Kohara Y, Hasebe M (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci USA 100:8007–8012
Ober D (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends Plant Sci 10:444–449
Paniego NB, Zuurbier KW, Fung SY, van der Heijden R, Scheffer JJ, Verpoorte R (1999) Phlorisovalerophenone synthase, a novel polyketide synthase from hop (Humulus lupulus L.) cones. Eur J Biochem 262:612–616
Qian W, Tan G, Liu H, He S, Gao Y, An C (2007) Identification of a bHLH-type G-box binding factor and its regulation activity with G-box and Box I elements of the PsCHS1 promoter. Plant Cell Rep 26:85–93
Quatrano RS, McDaniel SF, Khandelwal A, Perroud PF, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10:182–189
Rensing SA, Fritzowsky D, Lang D, Reski R (2005) Protein encoding genes in an ancient plant: analysis of codon usage, retained genes and splice sites in a moss, Physcomitrella patens. BMC Genomics 6:43
Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R (2007) An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol 7:130–139
Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538
Schröder J (1997) A family of plant-specific polyketide synthases: facts and predictions. Trends Plant Sci 2:373–378
Seshime Y, Juvvadi PR, Fujii I, Kitamoto K (2005) Discovery of a novel superfamily of type III polyketide synthases in Aspergillus oryzae. Biochem Biophys Res Commun 331:253–260
Sommer H, Saedler H (1986) Structure of the chalcone synthase gene of Antirrhinum majus. Mol Gen Genet 202:429–434
Spalding JB, Lammers PJ (2004) BLAST Filter and GraphAlign: rule-based formation and analysis of sets of related DNA and protein sequences. Nucleic Acids Res 32:W26–W32
Stafford HA (1991) Flavonoid evolution: an enzymic approach. Plant Physiol 96:680–685
Staiger D, Kaulen H, Schell J (1989) A CACGTG motif of the Antirrhinum majus chalcone synthase promoter is recognized by an evolutionarily conserved nuclear protein. Proc Natl Acad Sci USA 86:6930–6934
Suh D-Y, Fukuma K, Kagami J, Yamazaki Y, Shibuya M, Ebizuka Y, Sankawa U (2000a) Identification of amino acid residues important in the cyclization reactions of chalcone and stilbene synthases. Biochem J 350:229–235
Suh D-Y, Kagami J, Fukuma K, Sankawa U (2000b) Evidence for catalytic cysteine-histidine dyad in chalcone synthase. Biochem Biophys Res Commun 275:725–730
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Trapp SC, Croteau RB (2001) Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811–832
Trognitz F, Manosalva P, Gysin R, Niñio-Liu D, Simon R, del Herrera MR, Trognitz B, Ghislain M, Nelson R (2002) Plant defense genes associated with quantitative resistance to potato late blight in Solanum phureja × dihaploid S. tuberosum hybrids. Mol Plant Microbe Interact 15:587–597
Wingender R, Röhrig H, Höricke C, Wing D, Schell J (1989) Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Mol Gen Genet 218:315–322
Wu S, O’Leary SJ, Gleddie S, Eudes F, Laroche A, Robert LS (2008) A chalcone synthase-like gene is highly expressed in the tapetum of both wheat (Triticum aestivum L.) and triticale (×Triticosecale Wittmack). Plant Cell Rep 27:1441–1449
Yamazaki Y, Suh D-Y, Sitthithaworn W, Ishiguro K, Kobayashi Y, Shibuya M, Ebizuka Y, Sankawa U (2001) Diverse chalcone synthase superfamily enzymes from the most primitive vascular plant, Psilotum nudum. Planta 214:75–84
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298
Acknowledgments
This research was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) and the University of Regina. E. I. B. and C. C. C. are recipients of NSERC postgraduate scholarships (PGS-D and CGS-M, respectively).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Koduri, P.K.H., Gordon, G.S., Barker, E.I. et al. Genome-wide analysis of the chalcone synthase superfamily genes of Physcomitrella patens . Plant Mol Biol 72, 247–263 (2010). https://doi.org/10.1007/s11103-009-9565-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-009-9565-z