Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus

Planta

Volumn 236, Issue 5, 2012, Pages 1571-1581

  Huang, Lili ^a,b,c   Li, Jia ^a   Ye, Hechun ^b   Li, Changfu ^a   Wang, Hong ^c   Liu, Benye ^b   Zhang, Yansheng ^a  

^a Wuhan Institute of Botany Chinese Academy of Sciences   (China)

^b INSTITUTE OF BOTANY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

C 28 Oxidase; CYP716AL1; Oleanolic acid; Triterpene synthase; Ursolic acid

Indexed keywords

AMYRIN; COMPLEMENTARY DNA; CYTOCHROME P450; DRUG DERIVATIVE; LANOSTEROL SYNTHASE; LUPEOL; MUTASE; OLEANOLIC ACID; PENTACYCLIC TRITERPENE; TRITERPENE; URSOLIC ACID; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CATHARANTHUS; EXPRESSED SEQUENCE TAG; GENE EXPRESSION REGULATION; GENETICS; MEDICINAL PLANT; METABOLISM; MOLECULAR CLONING; PLANT LEAF; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; BIOSYNTHETIC PATHWAYS; CATHARANTHUS; CLONING, MOLECULAR; CYTOCHROME P-450 ENZYME SYSTEM; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION, PLANT; INTRAMOLECULAR TRANSFERASES; OLEANOLIC ACID; PENTACYCLIC TRITERPENES; PLANT LEAVES; PLANT PROTEINS; PLANTS, MEDICINAL; SACCHAROMYCES CEREVISIAE; TRITERPENES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CATHARANTHUS ROSEUS; SACCHAROMYCES CEREVISIAE;

EID: 84868091024     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1712-0     Document Type: Article

References (48)

1. Abe I, Rohmer M, Prestwich GD (1993) Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem Rev 93: 2189-2206.
2. Augustin JM, Kuzina V, Andersen SB, Bak S (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72: 435-457.
3. Basyuni M, Oku H, Inafuku M, Baba S, Iwasaki H, Oshiro K, Okabe T, Shibuya M, Ebizuka Y (2006) Molecular cloning and functional expression of a multifunctional triterpene synthase cDNA from a mangrove species Kandelia candel (L.) Druce. Phytochemistry 67: 2517-2524.
4. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54: 656-669.
5. Brendolise C, Yauk Y-K, Eberhard ED, Wang M, Chagne D, Andre C, Greenwood DR, Beuning LL (2011) An unusual plant triterpene synthase with predominant α-amyrin producing activity identified by characterising oxidosqualene cyclases from Malus × domestica. FEBS J 278: 2485-2499.
6. Bringe K, Schumacher CFA, Schmitz-Eiberger M, Steiner U, Oerke E-C (2006) Ontogenetic variation in chemical and physical characteristics of adaxial apple leaf surfaces. Phytochemistry 67: 161-170.
7. Carelli M, Biazzi E, Panara F, Tava A, Scaramelli L, Porceddu A, Graham N, Odoardi M, Piano E, Arcioni S, May S, Scotti C, Calderini O (2011) Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell 23: 3070-3081.
8. El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6: 277-305.
9. Farina C, Pinza M, Pifferi G (1998) Synthesis and anti-ulcer activity of new derivatives of glycyrrhetic, oleanolic and ursolic acids. Il Farmaco 53: 22-32.
10. Fazio GC, Xu R, Matsuda SP (2004) Genome mining to identify new plant triterpenoids. J Am Chem Soc 126: 5678-5679.
11. Fukushima EO, Seki H, Ohyama K, Ono E, Umemoto N, Mizutani M, Saito K, Muranaka T (2011) CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis. Plant Cell Physiol 52: 2050-2061.
12. Fulda S (2008) Betulinic acid for cancer treatment and prevention. Int J Mol Sci 9: 1096-1107.
13. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96.
14. Grncarevic M, Radler F (1971) A review of the surface lipids of grapes and their importance in the drying process. AM J Enol Vitic 20: 80-86.
15. Guhling O, Hobl B, Yeats T, Jetter R (2006) Cloning and characterization of a lupeol synthase involved in the synthesis of epicuticular wax crystals on stem and hypocotyl surfaces of Ricinus communis. Arch Biochem Biophys 448: 60-72.
16. Hayashi H, Hiraoka N, Ikeshiro Y, Kushiro T, Morita M, Shibuya M, Ebizuka Y (2000) Molecular cloning and characterization of a cDNA for Glycyrrhiza glabra cycloartenol synthase. Biol Pharm Bull 23: 231-234.
17. Hayashi H, Huang P, Inoue K, Hiraoka N, Ikeshiro Y, Yazaki K, Tanaka S, Kushiro T, Shibuya M, Ebizuka Y (2001) Molecular cloning and characterization of isomultiflorenol synthase, a new triterpene synthase from Luffa cylindrica, involved in biosynthesis of bryonolic acid. Eur J Biochem 268: 6311-6317.
18. Helliwell CA, Poole A, Peacock WJ, Dennis ES (1999) Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol 119: 507-510.
19. Herrera JB, Bartel B, Wilson WK, Matsuda SP (1998) Cloning and characterization of the Arabidopsis thaliana lupeol synthase gene. Phytochemistry 49: 1905-1911.
20. Husselstein-Muller T, Schaller H, Benveniste P (2001) Molecular cloning and expression in yeast of 2, 3-oxidosqualene-triterpenoid cyclases from Arabidopsis thaliana. Plant Mol Biol 45: 75-92.
21. Kajikawa M, Yamato KT, Fukuzawa H, Sakai Y, Uchida H, Ohyama K (2005) Cloning and characterization of a cDNA encoding beta-amyrin synthase from petroleum plant Euphorbia tirucalli L. Phytochemistry 66: 1759-1766.
22. Kirby J, Romanini DW, Paradise EM, Keasling JD (2008) Engineering triterpene production in Saccharomyces cerevisiae-beta-amyrin synthase from Artemisia annua. FEBS J 275: 1852-1859.
23. Kushiro T, Shibuya M, Ebizuka Y (1998) β-Amyrin synthase cloning of oxidosqualene cyclase that catalyzes the formation of the most popular triterpene among higher plants. Eur J Biochem 256: 238-244.
24. Liu J (1995) Pharmacology of oleanolic acid and ursolic acid. J Ethnopharmacol 49: 57-68.
25. Liu J (2005) Oleanolic acid and ursolic acid: research perspectives. J Ethnopharmacol 100: 92-94.
26. Liu YG, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25: 674-681.
27. Morita M, Shibuya M, Kushiro T, Masuda K, Ebizuka Y (2000) Molecular cloning and functional expression of triterpene synthases from pea. Eur J Biochem 267: 3453-3460.
28. Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20: 524-542.
29. O'Connor SE, Maresh JJ (2006) Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat Prod Rep 23: 532-547.
30. Pereira SI, Freire CSR, Pascoal Neto C, Silvestre AJD, Silva AMS (2005) Chemical composition of the epicuticular wax from the fruits of Eucalyptus globulus. Phytochem Anal 16: 364-369.
31. Phillips DR, Rasbery JM, Bartel B, Matsuda SPT (2006) Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 9: 305-314.
32. Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272: 51-64.
33. Qi X, Bakht S, Qin B, Leggett M, Hemmings A, Mellon F, Eagles J, Werck-Reichhart D, Schaller H, Lesot A, Melton R, Osbourn A (2006) A different function for a member of an ancient and highly conserved cytochrome P450 family: from essential sterols to plant defense. Proc Natl Acad Sci USA 103: 18848-18853.
34. Reiling KK, Yoshikuni Y, Martin VJJ, Newman J, Bohlmann J, Keasling JD (2004) Mono and diterpene production in Escherichia coli. Biotechnol Bioeng 87: 200-212.
35. Ro D, Arimura G, Lau S, Piers E, Bohlmann J (2005) Loblolly pine abietadienol/abietadienal oxidase PtAO (CYP720B1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. Proc Natl Acad Sci USA 102: 8060-8065.
36. Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940-943.
37. Seki H, Ohyama K, Sawai S, Mizutani M, Ohnishi T, Sudo H, Akashi T, Aoki T, Saito K, Muranaka T (2008) Licorice β-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc Natl Acad Sci USA 105: 14204-14209.
38. Shibuya M (2004) Cucurbitadienol synthase, the first committed enzyme for cucurbitacin biosynthesis, is a distinct enzyme from cycloartenol synthase for phytosterol biosynthesis. Tetrahedron 60: 6995-7003.
39. Shibuya M, Zhang H, Endo A, Shishikura K, Kushiro T, Ebizuka Y (1999) Two branches of the lupeol synthase gene in the molecular evolution of plant oxidosqualene cyclases. Eur J Biochem 266: 302-307.
40. Shibuya M, Hoshino M, Katsube Y, Hayashi H, Kushiro T, Ebizuka Y (2006) Identification of beta-amyrin and sophoradiol 24-hydroxylase by expressed sequence tag mining and functional expression assay. FEBS J 273: 948-959.
41. Shibuya M, Katsube Y, Otsuka M, Zhang H, Tansakul P, Xiang T, Ebizuka Y (2009) Identification of a product specific beta-amyrin synthase from Arabidopsis thaliana. Plant Physiol Biochem 47: 26-30.
42. Smimaru H, Orihara Y, Tansakul P, Kang YH, Shibuya MYE (2007) Production of triterpene acids by cell suspension cultures of Olea europaea. Chem Pharm Bull 55: 784-788.
43. Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS (2006) Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett 580: 1411-1416.
44. Usia T, Watabe T, Kadota S, Tezuka Y (2005) Cytochrome P450 2D6 (CYP2D6) inhibitory constituents of Catharanthus roseus. Biol Pharm Bull 28: 1021-1024.
45. van der Heijden R, Jacobs DI, Snoeijer W, Hallared D, Verpoorte R (2004) The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11: 607-628.
46. Wang Z, Guhling O, Yao R, Li F, Yeats TH, Rose JKC, Jetter R (2010) Two oxidosqualene cyclases responsible for biosynthesis of tomato fruit cuticular triterpenoids. Plant Physiol 155: 540-552.
47. Xiong Q, Wilson WK, Matsuda SP (2006) An Arabidopsis oxidosqualene cyclase catalyzes iridal skeleton formation by Grob fragmentation. Angew Chem Int Ed Engl 45: 1285-1288.
48. Yu MML, Konorov SO, Schulze HG, Blades MW, Turner RFB, Jetter R (2007) In situ analysis by microspectroscopy reveals triterpenoid compositional patterns within leaf cuticles of Prunus laurocerasus. Planta 227: 823-834.