Genome-wide analysis of the chalcone synthase superfamily genes of Physcomitrella patens

Plant Molecular Biology

Volumn 72, Issue 3, 2010, Pages 247-263

  Koduri, P K Harshavardhan ^a   Gordon, Graeme S ^a   Barker, Elizabeth I ^a   Colpitts, Che C ^a   Ashton, Neil W ^a   Suh, Dae Yeon ^a  

^a UNIVERSITY OF REGINA   (Canada)

Author keywords

Chalcone synthase superfamily; Cis acting elements; Enzyme evolution; Gene duplication; Gene regulation; Multigene family; Physcomitrella patens; Retrotransposition

Indexed keywords

ACYLTRANSFERASE; CHALCONE SYNTHASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BRYOPSIDA; DNA SEQUENCE; ENZYMOLOGY; EXPRESSED SEQUENCE TAG; GENE DUPLICATION; GENE EXPRESSION; GENETICS; INTRON; LIGHT; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PLANT GENOME; RADIATION EXPOSURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; BRYOPSIDA; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE DUPLICATION; GENE EXPRESSION; GENOME, PLANT; INTRONS; LIGHT; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PLANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN;

BACTERIA (MICROORGANISMS); BRYOPHYTA; EMBRYOPHYTA; FUNGI; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 75949100048     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-009-9565-z     Document Type: Article

References (79)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Austin MB, Noel JP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20: 79-110.
8. 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.
9. 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.
10. 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.
11. Brinkmeier E, Geiger H, Zinsmeister HD (1999) Biflavonoids and 4, 2′-epoxy-3-phenylcoumarins from the moss Mnium hornum. Phytochemistry 52: 297-302.
12. 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.
13. Dipp NJ, Newman AJ (1989) Evidence that introns arose at proto-splice site. EMBO J 8: 2015-2021.
14. Domínguez E, Mercado JA, Quesada MA, Heredia A (1999) Pollen sporopollenin: degradation and structural elucidation. Sex Plant Reprod 12: 171-178.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. Fujita Y (1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol 37: 411-421.
21. 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.
22. 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.
23. 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.
24. Geiger H, Markham KR (1992) Campylopusaurone, an auronoflavanone biflavonoid from the mosses Campylopus clavatus and Campylopus holomitrium. Phytochemistry 31: 4325-4328.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Iwashina T (2000) The structure and distribution of the flavonoids in plants. J Plant Res 113: 287-299.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. Jiang C, Kim SY, Suh D-Y (2008) Divergent evolution of the thiolase superfamily and chalcone synthase family. Mol Phylogenet Evol 49: 691-701.
38. Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41: 577-585.
39. Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35: 993-1001.
40. Kamisugi Y, Cuming AC, Cove DJ (2005) Parameters determining the efficiency of gene targeting in the moss Physcomitrella patens. Nucleic Acids Res 33: e173.
41. 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.
42. 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.
43. Kumar S, Tamura K, Nei M (2004) MEGA3: Intergrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
44. 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.
45. 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.
46. 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.
47. Liu B, Raeth T, Beuerle T, Beerhues L (2007) Biphenyl synthase, a novel type III polyketide synthase. Planta 225: 1495-1503.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. Ober D (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends Plant Sci 10: 444-449.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
64. Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6: 526-538.
65. Schröder J (1997) A family of plant-specific polyketide synthases: facts and predictions. Trends Plant Sci 2: 373-378.
66. 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.
67. Sommer H, Saedler H (1986) Structure of the chalcone synthase gene of Antirrhinum majus. Mol Gen Genet 202: 429-434.
68. 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.
69. Stafford HA (1991) Flavonoid evolution: an enzymic approach. Plant Physiol 96: 680-685.
70. 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.
71. 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.
72. 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.
73. 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.
74. Trapp SC, Croteau RB (2001) Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158: 811-832.
75. 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.
76. 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.
77. 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.
78. 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.
79. Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18: 292-298.