Identification of key amino acid residues determining product specificity of 2,3-oxidosqualene cyclase in Oryza species

New Phytologist

Volumn 218, Issue 3, 2018, Pages 1076-1088

  Xue, Zheyong ^a,b   Tan, Zhengwei ^a,c,d   Huang, Ancheng ^b   Zhou, Yuan ^a,c   Sun, Juncong ^a,c   Wang, Xiaoning ^e   Thimmappa, Ramesha B ^b   Stephenson, Michael J ^b   Osbourn, Anne ^b   Qi, Xiaoquan ^a  

^a INSTITUTE OF BOTANY   (China)

^b NORWICH RESEARCH PARK   (United Kingdom)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e SHANDONG UNIVERSITY   (China)

Author keywords

chemical diversity; conformation; orysatinol; oxidosqualene cyclase (OSC); parkeol; product specificity; rice; triterpene

Indexed keywords

AMINO ACID; CHEMICAL ANALYSIS; ENZYME; GRASS; IDENTIFICATION KEY; PHYLOGENETICS; RICE; SUBSPECIES;

JAPONICA; ORYZA; ORYZA SATIVA; ZIZANIA;

AMINO ACID; LANOSTEROL; LANOSTEROL SYNTHASE; MUTASE; PARKEOL;

AMINO ACID SEQUENCE; CHEMISTRY; CYCLIZATION; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC VARIATION; GENETICS; METABOLISM; ORYZA; PHYLOGENY;

AMINO ACID SEQUENCE; AMINO ACIDS; CYCLIZATION; GENETIC VARIATION; INTRAMOLECULAR TRANSFERASES; LANOSTEROL; ORYZA; PHYLOGENY; SUBSTRATE SPECIFICITY;

EID: 85043479804     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.15080     Document Type: Article

References (40)

1. Augustin JM, Kuzina V, Andersen SB, Bak S. 2011. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72: 435–457.
2. Banta AB, Wei JH, Gill CC, Giner JL, Welander PV. 2016. Synthesis of arborane triterpenols by a bacterial oxidosqualene cyclase. Proceedings of the National Academy of Sciences, USA 114: 245–250.
3. Benveniste P. 1986. Sterol biosynthesis. Annual Review of Plant Physiology 37: 275–308.
4. Bergelson J, Kreitman M, Stahl EA, Tian D. 2001. Evolutionary dynamics of plant R-genes. Science 292: 2281–2285.
5. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L et al. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42: W252–W258.
6. Bishop GJ, Koncz C. 2002. Brassinosteroids and plant steroid hormone signaling. Plant Cell 14: S97–S110.
7. Bloch K. 1965. The biological synthesis of cholesterol. Vitamins and Hormones 15: 119–150.
8. Chang CH, Chen YC, Tseng SW, Liu YT, Wen HY, Li WH, Huang CY, Ko CY, Wang TT, Wu TK. 2012. The cysteine 703 to isoleucine or histidine mutation of the oxidosqualene-lanosterol cyclase from Saccharomyces cerevisiae generates an iridal-type triterpenoid. Biochimie 94: 2376–2381.
9. Chappell J. 2002. The genetics and molecular genetics of terpene and sterol origami. Current Opinion in Plant Biology 5: 151–157.
10. Christianson DW. 2006. Structural biology and chemistry of the terpenoid cyclases. Chemical Reviews 106: 3412–3442.
11. Hart EA, Ling H, Darr LB, Wilson WK, Pang JA, Matsuda SPT. 1999. Directed evolution to investigate steric control of enzymatic oxidosqualene cyclization. An isoleucine-to-valine mutation in cycloartenol synthase allows lanosterol and parkeol biosynthesis. Journal of the American Chemical Society 121: 9887–9888.
12. Herrera JBR, Wilson WK, Matsuda SPT. 2000. A tyrosine-to-threonine mutation converts cycloartenol synthase to an oxidosqualene cyclase that forms lanosterol as its major product. Journal of the American Chemical Society 122: 6765–6766.
13. Huang XH, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W et al. 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature 490: 497–501.
14. Inagaki YS, Etherington G, Geisler K, Field B, Dokarry M, Ikeda K, Mutsukado Y, Dicks J, Osbourn A. 2011. Investigation of the potential for triterpene synthesis in rice through genome mining and metabolic engineering. New Phytologist 191: 432–448.
15. Ito R, Hashimoto I, Masukawa Y, Hoshino T. 2013. Effect of cation-π interactions and steric bulk on the catalytic action of oxidosqualene cyclase: a case study of phe 728 of β-amyrin synthase from Euphorbia tirucalli L. Chemistry – A European Journal 19: 17150–17158.
16. Ito R, Mori K, Hashimoto I, Nakano C, Sato T, Hoshino T. 2011. Triterpene cyclases from Oryza sativa L.: cycloartenol, parkeol and achilleol B synthases. Organic Letters 13: 2678–2681.
17. Kovach MJ, Sweeney MT, McCouch SR. 2007. New insights into the history of rice domestication. Trends in Genetics 23: 578–587.
18. Matsuda SPT, Darr LB, Hart EA, Herrera JBR, McCann KE, Meyer MM, Pang J, Schepmann HG. 2000. Steric bulk at cycloartenol synthase position 481 influences cyclization and deprotonation. Organic Letters 2: 2261–2263.
19. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. Journal of Computational Chemistry 30: 2785–2791.
20. Moses T, Papadopoulou KK, Osbourn A. 2014. Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives. Critical Reviews in Biochemistry and Molecular Biology 49: 439–462.
21. Ohyama K, Suzuki M, Kikuchi J, Saito K, Muranaka T. 2009. Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 725–730.
22. Osbourn A, Goss RJM, Field RA. 2011. The saponins – polar isoprenoids with important and diverse biological activities. Natural Products Reports 28: 1261–1268.
23. Parks LW, Casey WM. 1995. Physiological implications of sterol biosynthesis in Yeast. Annual Review of Microbiology 49: 95–116.
24. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera – a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25: 1605–1612.
25. Salmon M, Thimmappaa RB, Minto RE, Melton RE, Hughes RK, O'Maille PE, Hemmings AM, Osbourn A. 2016. A conserved amino acid residue critical for product and substrate specificity in plant triterpene synthases. Proceedings of the National Academy of Sciences, USA 113: E4407–E4414.
26. Sang T, Ge S. 2007. The puzzle of rice domestication. Journal of Integrative Plant Biology 49: 760–768.
27. Sun JC, Xu X, Xue ZY, Snyder JH, Qi XQ. 2013. Functional analysis of a rice oxidosqualene cyclase through total gene synthesis. Molecular Plant 6: 1726–1729.
28. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
29. Thimmappa R, Geisler K, Louveau T, O'Maille P, Osbourn A. 2014. Triterpene biosynthesis in plants. Annual Review of Plant Biology 65: 225–257.
30. Thoma R, Schulz-Gasch T, D'Arcy B, Benz J, Aebi J, Dehmlow H, Hennig M, Stihle M, Ruf A. 2004. Insight into steroid scaffold formation from the structure of human oxidosqualene cyclase. Nature 432: 118–122.
31. Weng JK. 2014. The evolutionary paths towards complexity: a metabolic perspective. New Phytologist 201: 1141–1149.
32. Wu TK, Chang CH, Liu YT, Wang TT. 2008. Saccharomyces cerevisiae oxidosqualene-lanosterol cyclase: a chemistry–biology interdisciplinary study of the protein's structure-function-reaction mechanism relationships. Chemical Record 8: 302–325.
33. Wu TK, Griffin JH. 2002. Conversion of a plant oxidosqualene-cycloartenol synthase to an oxidosqualene-lanosterol cyclase by random mutagenesis. Biochemistry 41: 8238–8244.
34. Wu TK, Liu YT, Chang CH. 2005. Histidine residue at position 234 of oxidosqualene-lanosterol cyclase from Saccharomyces cerevisiae simultaneously influences cyclization, rearrangement, and deprotonation reactions. ChemBioChem 6: 1177–1181.
35. Wu TK, Liu YT, Chang CH, Yu MT, Wang HJ. 2006. Site-saturated mutagenesis of histidine 234 of Saccharomyces cerevisiae oxidosqualene-lanosterol cyclase demonstrates dual functions in cyclization and rearrangement reactions. Journal of the American Chemical Society 128: 6414–6419.
36. Xiong QB, Wilson WK, Matsuda SPT. 2006. An Arabidopsis oxidosqualene cyclase catalyzes iridal skeleton formation by Grob fragmentation. Angewandte Chemie. International Edition 45: 1285–1288.
37. Xu MM, Wilderman PR, Peters RJ. 2007. Following evolution's lead to a single residue switch for diterpene synthase product outcome. Proceedings of the National Academy of Sciences, USA 104: 7397–7401.
38. Xu R, Fazio GC, Matsuda SPT. 2004. On the origins of triterpenoid skeletal diversity. Phytochemistry 65: 261–291.
39. Xue Z, Duan L, Liu D, Guo J, Ge S, Dicks J, ÓMáille P, Osbourn A, Qi X. 2012. Divergent evolution of oxidosqualene cyclases in plants. New Phytologist 193: 1022–1038.
40. Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586–1591.