The remarkable pliability and promiscuity of specialized metabolism

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 77, Issue , 2012, Pages 309-320

  Weng, J K ^a   Noel, J P ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; STRICTOSIDINE SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL FUNCTION; DYNAMICS; ECOSYSTEM; ENZYME STRUCTURE; GENETIC VARIABILITY; HOMEOSTASIS; METABOLISM; METABOLITE; ORGANISMS; PHYLOGENY; PLIABILITY; PRESSURE; PRIORITY JOURNAL; SURVIVAL; ABIOTIC STRESS; BIOTIC STRESS; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE; GENOME; GENOMICS; MOLECULAR DYNAMICS; NONHUMAN; SPECIES DIVERSITY; STOICHIOMETRY;

BIOCATALYSIS; ENZYMES; EVOLUTION, MOLECULAR; GENETIC VARIATION; HOMEOSTASIS; METABOLIC NETWORKS AND PATHWAYS;

EID: 84881488183     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2012.77.014787     Document Type: Article

References (107)

1. Achnine L, Blancaflor EB, Rasmussen S, Dixon RA. 2004. Colocalization of L-phenylalanine ammonialyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16: 3098-3109.
2. Andreasson E, Bolt Jorgensen L, Hoglund AS, Rask L, Meijer J. 2001. Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiol 127: 1750-1763.
3. Auldridge ME, Guo Y, Austin MB, Ramsey J, Fridman E, Pichersky E, Noel JP. 2012. Emergent decarboxylase activity and attenuation of α/β-hydrolase activity during the evolution of methylketone biosynthesis in tomato. Plant Cell 24: 1596-1607.
4. Austin MB, Noel JP. 2003. The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20: 79-110.
5. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011a. The family of terpene synthases in plants: A midsize family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66: 212-229.
6. Chen HC, Li Q, Shuford CM, Liu J, Muddiman DC, Sederoff RR, Chiang VL. 2011b. Membrane protein complexes catalyze both 4-and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis. Proc Natl Acad Sci 108: 21253-21258.
7. Chu HY, Wegel E, Osbourn A. 2011. From hormones to secondary metabolism: The emergence of metabolic gene clusters in plants. Plant J 66: 66-79.
8. Cook PF, Cleland WW. 2007. Enzyme kinetics and mechanism. Garland Science, London; New York.
9. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9: e0156.
10. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR. 2012. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci 109: E2183-E2191.
11. Earl DJ, Deem MW. 2004. Evolvability is a selectable trait. Proc Natl Acad Sci 101: 11531-11536.
12. Eckert AJ, Wegrzyn JL, Cumbie WP, Goldfarb B, Huber DA, Tolstikov V, Fiehn O, Neale DB. 2011. Association genetics of the loblolly pine (Pinus taeda, Pinaceae) metabolome. New Phytol 193: 890-902.
13. Eisenmesser EZ, Bosco DA, Akke M, Kern D. 2002. Enzyme dynamics during catalysis. Science 295: 1520-1523.
14. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D. 2005. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438: 117-121.
15. Fernstrom JD, Fernstrom MH. 1994. Dietary effects on tyrosine availability and catecholamine synthesis in the central nervous system: Possible relevance to the control of protein intake. Proc Nutr Soc 53: 419-429.
16. Firn RD, Jones CG. 2009. A Darwinian view of metabolism: Molecular properties determine fitness. J Exp Bot 60: 719-726.
17. Fleet CM, Sun TP. 2005. A DELLAcate balance: The role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8: 77-85.
18. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, et al. 2005. Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci 102: 1773-1778.
19. Fraenkel GS. 1959. The raison d'etre of secondary plant substances; these odd chemicals arose as a means of protecting plants from insects and now guide insects to food. Science 129: 1466-1470.
20. Franken SM, Rozeboom HJ, Kalk KH, Dijkstra BW. 1991. Crystal structure of haloalkane dehalogenase: An enzyme to detoxify halogenated alkanes. EMBO J 10: 1297-1302.
21. Fraser CM, Thompson MG, Shirley AM, Ralph J, Schoenherr JA, Sinlapadech T, Hall MC, Chapple C. 2007. Related Arabidopsis serine carboxypeptidase-like sinapoylglucose acyltransferases display distinct but overlapping substrate specificities. Plant Physiol 144: 1986-1999.
22. Fujioka S, Yokota T. 2003. Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54: 137-164.
23. Gagne SJ, Stout JM, Liu E, Boubakir Z, Clark SM, Page JE. 2012. Identification of olivetolic acid cyclase from Cannabis sativa reveals a unique catalytic route to plant polyketides. Proc Natl Acad Sci 109: 12811-12816.
24. Gang DR. 2005. Evolution of flavors and scents. Annu Rev Plant Biol 56: 301-325.
25. Goldsmith M, Tawfik DS. 2012. Directed enzyme evolution: Beyond the low-hanging fruit. Curr Opin Struct Biol 22: 406-412.
26. Gruber K, Gartler G, Krammer B, Schwab H, Kratky C. 2004. Reaction mechanism of hydroxynitrile lyases of the alpha/β-hydrolase superfamily: The threedimensional structure of the transient enzymesubstrate complex certifies the crucial role of LYS236. J Biol Chem 279: 20501-20510.
27. Halabi N, Rivoire O, Leibler S, Ranganathan R. 2009. Protein sectors: Evolutionary units of threedimensional structure. Cell 138: 774-786.
28. Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57: 303-333.
29. Henzler-Wildman K, Kern D. 2007. Dynamic personalities of proteins. Nature 450: 964-972.
30. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D. 2007. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450: 913-916.
31. Hrmova M, De Gori R, Smith BJ, Fairweather JK, Driguez H, Varghese JN, Fincher GB. 2002. Structural basis for broad substrate specificity in higher plant β-D-glucan glucohydrolases. Plant Cell 14: 1033-1052.
32. Huang FC, Horvath G, Molnar P, Turcsi E, Deli J, Schrader J, Sandmann G, Schmidt H, Schwab W. 2009. Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena. Phytochemistry 70: 457-464.
33. Huang R, Hippauf F, Rohrbeck D, Haustein M, Wenke K, Feike J, Sorrelle N, Piechulla B, Barkman TJ. 2012. Enzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates. Proc Natl Acad Sci 109: 2966-2971.
34. Jones JE. 1924. On the determination of molecular fields. II. From the equation of state of a gas. Proc R Soc Lond A 106: 463-477.
35. Jones CG, Firn RD, Malcolm SB. 1991. On the evolution of plant secondary chemical diversity [and Discussion]. Philos Trans R Soc Lond B Biol Sci 333: 273-280.
36. Jorgensen K, Rasmussen AV, Morant M, Nielsen AH, Bjarnholt N, Zagrobelny M, Bak S, Moller BL. 2005. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr Opin Plant Biol 8: 280-291.
37. Kashtan N, Noor E, Alon U. 2007. Varying environments can speed up evolution. Proc Natl Acad Sci 104: 13711-13716.
38. Khersonsky O, Tawfik DS. 2010. Enzyme promiscuity: A mechanistic and evolutionary perspective. Annu Rev Biochem 79: 471-505.
39. Kienow L, Schneider K, Bartsch M, Stuible HP, Weng H, Miersch O, Wasternack C, Kombrink E. 2008. Jasmonates meet fatty acids: Functional analysis of a new acylcoenzyme A synthetase family from Arabidopsis thaliana. J Exp Bot 59: 403-419.
40. Kim SJ, Kim MR, Bedgar DL, Moinuddin SG, Cardenas CL, Davin LB, Kang C, Lewis NG. 2004. Functional reclassification of the putative cinnamyl alcohol dehydrogenase multigene family in Arabidopsis. Proc Natl Acad Sci 101: 1455-1460.
41. Kirk H, Macel M, Klinkhamer PGL, Vrieling K. 2004. Natural hybridization between Senecio jacobaea and Senecio aquaticus: Molecular and chemical evidence. Mol Ecol 13: 2267-2274.
42. Kirk H, Choi YH, Kim HK, Verpoorte R, van der Meijden E. 2005. Comparing metabolomes: The chemical consequences of hybridization in plants. New Phytol 167: 613-622.
43. Kirk H, Cheng D, Choi YH, Vrieling K, Klinkhamer PG. 2012. Transgressive segregation of primary and secondary metabolites in F2 hybrids between Jacobaea aquatica and J. vulgaris. Metabolomics 8: 211-219.
44. Kliebenstein DJ. 2008. A role for gene duplication and natural variation of gene expression in the evolution of metabolism. PLoS One 3: e1838.
45. 2+;-dependent O-methyltransferases. J Mol Biol 378: 154-164.
46. Kühne W. 1877. Über das Verhalten verschiedener organisirterund sog. ungeformter Fermente. Verh naturhmed Ver Heidelb 1: 190-193.
47. Kumano T, Tomita T, Nishiyama M, Kuzuyama T. 2010. Functional characterization of the promiscuous prenyltransferase responsible for furaquinocin biosynthesis: Identification of a physiological polyketide substrate and its prenylated reaction products. J Biol Chem 285: 39663-39671.
48. Kumar D, Klessig DF. 2003. Highaffinity salicylic acidbinding protein 2 is required for plant innate immunity and has salicylic acidstimulated lipase activity. Proc Natl Acad Sci 100: 16101-16106.
49. Kunzler DE, Sasso S, Gamper M, Hilvert D, Kast P. 2005. Mechanistic insights into the isochorismate pyruvate lyase activity of the catalytically promiscuous PchB from combinatorial mutagenesis and selection. J Biol Chem 280: 32827-32834.
50. Lamb AL. 2011. Pericyclic reactions catalyzed by chorismateutilizing enzymes. Biochemistry 50: 7476-7483.
51. Landmann C, Hucherig S, Fink B, Hoffmann T, Dittlein D, Coiner HA, Schwab W. 2011. Substrate promiscuity of a rosmarinic acid synthase from lavender (Lavandula angustifolia L.). Planta 234: 305-320.
52. Lee DS, Nioche P, Hamberg M, Raman CS. 2008. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455: 363-368.
53. Leivar P, Gonzalez VM, Castel S, Trelease RN, Lopez-Iglesias C, Arro M, Boronat A, Campos N, Ferrer A, Fernandez-Busquets X. 2005. Subcellular localization of Arabidopsis 3-hydroxy-3-methylglutarylcoenzyme A reductase. Plant Physiol 137: 57-69.
54. Li X, Bergelson J, Chapple C. 2010. The ARABIDOPSIS accession Pna-10 is a naturally occurring sng1 deletion mutant. Molecular Plant 3: 91-100.
55. Lim EK, Li Y, Parr A, Jackson R, Ashford DA, Bowles DJ. 2001. Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J Biol Chem 276: 4344-4349.
56. Lobkovsky AE, Wolf YI, Koonin EV. 2011. Predictability of evolutionary trajectories in fitness landscapes. PLoS Comput Biol 7: e1002302.
57. Ma X, Panjikar S, Koepke J, Loris E, Stockigt J. 2006. The structure of Rauvolfia serpentina strictosidine synthase is a novel six-bladed β-propeller fold in plant proteins. Plant Cell 18: 907-920.
58. Mao H, Williamson JR. 1999. Local folding coupled to RNA binding in the yeast ribosomal protein L30. J Mol Biol 292: 345-359.
59. Matsuno M, Compagnon V, Schoch GA, Schmitt M, Debayle D, Bassard JE, Pollet B, Hehn A, Heintz D, Ullmann P, et al. 2009. Evolution of a novel phenolic pathway for pollen development. Science 325: 1688-1692.
60. Merino E, Jensen RA, Yanofsky C. 2008. Evolution of bacterial trp operons and their regulation. Curr Opin Microbiol 11: 78-86.
61. Mintz-Oron S, Meir S, Malitsky S, Ruppin E, Aharoni A, Shlomi T. 2011. Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. Proc Natl Acad Sci 109: 339-344.
62. 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.
63. Nam H, Lewis NE, Lerman JA, Lee DH, Chang RL, Kim D, Palsson BO. 2012. Network context and selection in the evolution to enzyme specificity. Science 337: 1101-1104.
64. Nardini M, Ridder IS, Rozeboom HJ, Kalk KH, Rink R, Janssen DB, Dijkstra BW. 1999. The x-ray structure of epoxide hydrolase from Agrobacterium radiobacter AD1. An enzyme to detoxify harmful epoxides. J Biol Chem 274: 14579-14586.
65. Ngaki MN, Louie GV, Philippe RN, Manning G, Pojer F, Bowman ME, Li L, Larsen E, Wurtele ES, Noel JP. 2012. Evolution of the chalconeisomerase fold from fattyacid binding to stereospecific catalysis. Nature 485: 530-533.
66. Nielsen KA, Tattersall DB, Jones PR, Moller BL. 2008. Metabolon formation in dhurrin biosynthesis. Phytochemistry 69: 88-98.
67. Nishizawa T, Ueda A, Asayama M, Fujii K, Harada K, Ochi K, Shirai M. 2000. Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J Biochem 127: 779-789.
68. Oberhardt MA, Palsson BO, Papin JA. 2009. Applications of genome-scale metabolic reconstructions. Mol Syst Biol 5: 32O
69. O'Brien PJ, Herschlag D. 1999. Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol 6: R91-R105.
70. Ohnishi T, Godza B, Watanabe B, Fujioka S, Hategan L, Ide K, Shibata K, Yokota T, Szekeres M, Mizutani M. 2012. CYP90A1/CPD, a Brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C-3 oxidation. J Biol Chem 287: 31551-31560.
71. Okrent RA, Brooks MD, Wildermuth MC. 2009. Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J Biol Chem 284: 9742-9754.
72. O'Maille PE, Malone A, Dellas N, Andes Hess BJr, Smentek L, Sheehan I, Greenhagen BT, Chappell J, Manning G, Noel JP. 2008. Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat Chem Biol 4: 617-623.
73. Orians CM. 2000. The effects of hybridization in plants on secondary chemistry: Implications for the ecology and evolution of plantherbivore interactions. Am J Bot 87: 1749-1756.
74. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113-116.
75. Penn K, Jenkins C, Nett M, Udwary DW, Gontang EA, McGlinchey RP, Foster B, Lapidus A, Podell S, Allen EE, et al. 2009. Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria. ISME J 3: 1193-1203.
76. Pichersky E, Gang DR. 2000. Genetics and biochemistry of secondary metabolites in plants: An evolutionary perspective. Trends Plant Sci 5: 439-445.
77. Pichersky E, Lewinsohn E. 2011. Convergent evolution in plant specialized metabolism. Annu Rev Plant Biol 62: 549-566.
78. Pichersky E, Noel JP, Dudareva N. 2006. Biosynthesis of plant volatiles: Nature's diversity and ingenuity. Science 311: 808-811.
79. Prisic S, Peters RJ. 2007. Synergistic substrate inhibition of entcopalyl diphosphate synthase: A potential feed-forward inhibition mechanism limiting gibberellin metabolism. Plant Physiol 144: 445-454.
80. Quinsey NS, Luong AQ, Dickson PW. 1998. Mutational analysis of substrate inhibition in tyrosine hydroxylase. J Neurochem 71: 2132-2138.
81. Reed MC, Lieb A, Nijhout HF. 2010. The biological significance of substrate inhibition: A mechanism with diverse functions. Bioessays 32: 422-429.
82. Rétey J. 1990. Enzymic reaction selectivity by negative catalysis or how do enzymes deal with highly reactive intermediates? Angew Chem Int Ed Engl 29: 355-361.
83. Schneider K, Hovel K, Witzel K, Hamberger B, Schomburg D, Kombrink E, Stuible HP. 2003. The substrate specificity-determining amino acid code of 4-coumarate:CoA ligase. Proc Natl Acad Sci 100: 8601-8606.
84. Schneider K, Kienow L, Schmelzer E, Colby T, Bartsch M, Miersch O, Wasternack C, Kombrink E, Stuible HP. 2005. A new type of peroxisomal acylcoenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J Biol Chem 280: 13962-13972.
85. Sciara G, Kendrew SG, Miele AE, Marsh NG, Federici L, Malatesta F, Schimperna G, Savino C, Vallone B. 2003. The structure of ActVA-Orf6, a novel type of monooxygenase involved in actinorhodin biosynthesis. EMBO J 22: 205-215.
86. Shank EA, Kolter R. 2009. New developments in microbial interspecies signaling. Curr Opin Microbiol 12: 205-214.
87. Shevelev IV, Hubscher U. 2002. The 30 50 exonucleases. Nat Rev Mol Cell Biol 3: 364-376.
88. Thompson TB, Katayama K, Watanabe K, Hutchinson CR, Rayment I. 2004. Structural and functional analysis of tetracenomycin F2 cyclase from Streptomyces glaucescens. A type II polyketide cyclase. J Biol Chem 279: 37956-37963.
89. Tokuriki N, Tawfik DS. 2009a. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459: 668-673.
90. Tokuriki N, Tawfik DS. 2009b. Protein dynamism and evolvability. Science 324: 203-207.
91. Tudzynski B. 2005. Gibberellin biosynthesis in fungi: Genes, enzymes, evolution, and impact on biotechnology. Appl Microbiol Biotechnol 66: 597-611.
92. Vicente MF, Basilio A, Cabello A, Pelaez F. 2003. Microbial natural products as a source of antifungals. Clin Microbiol Infect 9: 15-32.
93. Vogt T. 2010. Phenylpropanoid biosynthesis. Mol Plant 3: 2-20.
94. Weid M, Ziegler J, Kutchan TM. 2004. The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci 101: 13957-13962.
95. Weinreich DM, Delaney NF, Depristo MA, Hartl DL. 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114.
96. Weng JK, Chapple C. 2010. The origin and evolution of lignin biosynthesis. New Phytol 187: 273-285.
97. Weng JK, Akiyama T, Ralph J, Chapple C. 2011. Independent recruitment of an O-methyltransferase for syringyl lignin biosynthesis in Selaginella moellendorffii. Plant Cell 23: 2708-2724.
98. Weng JK, Li Y, Mo H, Chapple C. 2012a. Assembly of an evolutionarily new pathway for α-pyrone biosynthesis in Arabidopsis. Science 337: 960-964.
99. Weng JK, Philippe RN, Noel JP. 2012b. The rise of chemodiversity in plants. Science 336: 1667-1670.
100. Werndl C. 2009. What are the new implications of chaos for unpredictability? Br J Philos Sci 60: 195-220.
101. Westfall CS, Zubieta C, Herrmann J, Kapp U, Nanao MH, Jez JM. 2012. Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336: 1708-1711.
102. Winkel BS. 2004. Metabolic channeling in plants. Annu Rev Plant Biol 55: 85-107.
103. Winzer T, Gazda V, He Z, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE, et al. 2012. A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336: 1704-1708.
104. Yoshikuni Y, Ferrin TE, Keasling JD. 2006. Designed divergent evolution of enzyme function. Nature 440: 1078-1082.
105. Zhou R, Jackson L, Shadle G, Nakashima J, Temple S, Chen F, Dixon RA. 2010. Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula. Proc Natl Acad Sci 107: 17803-17808.
106. Ziegler J, Facchini PJ. 2008. Alkaloid biosynthesis: Metabolism and trafficking. Annu Rev Plant Biol 59: 735-769.
107. Zubieta C, He XZ, Dixon RA, Noel JP. 2001. Structures of two natural product methyltransferases reveal the basis for substrate specificity in plant O-methyltransferases. Nat Struct Biol 8: 271-279.