Structural basis for divergent and convergent evolution of catalytic machineries in plant aromatic amino acid decarboxylase proteins

Torrens-Spence, Michael P.; Chiang, Ying-Chih; Smith, Tyler; Vicent, Maria A.; Wang, Yi; Weng, Jing-Ke

doi:10.1073/pnas.1920097117

Title: Structural basis for divergent and convergent evolution of catalytic machineries in plant aromatic amino acid decarboxylase proteins

Journal Article · Tue May 05 00:00:00 EDT 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1920097117· OSTI ID:1631858

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^[3]; Vicent, Maria A. ^[4]; Wang, Yi ^[2];

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Whitehead Inst. for Biomedical Research, Cambridge, MA (United States)
The Chinese Univ. of Hong Kong (Hong Kong)
Whitehead Inst. for Biomedical Research, Cambridge, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Whitehead Inst. for Biomedical Research, Cambridge, MA (United States); Williams College, Williamstown, MA (United States)

Radiation of the plant pyridoxal 5'-phosphate (PLP)-dependent aromatic L-amino acid decarboxylase (AAAD) family has yielded an array of paralogous enzymes exhibiting divergent substrate preferences and catalytic mechanisms. Plant AAADs catalyze either the decarboxylation or decarboxylation-dependent oxidative deamination of aromatic L-amino acids to produce aromatic monoamines or aromatic acetaldehydes, respectively. These compounds serve as key precursors for the biosynthesis of several important classes of plant natural products, including indole alkaloids, benzylisoquinoline alkaloids, hydroxycinnamic acid amides, phenylacetaldehyde-derived floral volatiles, and tyrosol derivatives. In this paper, we present the crystal structures of four functionally distinct plant AAAD paralogs. Through structural and functional analyses, we identify variable structural features of the substrate-binding pocket that underlie the divergent evolution of substrate selectivity toward indole, phenyl, or hydroxyphenyl amino acids in plant AAADs. Moreover, we describe two mechanistic classes of independently arising mutations in AAAD paralogs leading to the convergent evolution of the derived aldehyde synthase activity. Applying knowledge learned from this study, we successfully engineered a shortened benzylisoquinoline alkaloid pathway to produce (S)-norcoclaurine in yeast. This work highlights the pliability of the AAAD fold that allows change of substrate selectivity and access to alternative catalytic mechanisms with only a few mutations.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Pew Scholar Program in the Biomedical Sciences; Searle Scholars Program; National Science Foundation (NSF); Keck Foundation; The Chinese University of Hong Kong; National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: CHE-1709616; P41 GM103403; S10 RR029205; AC02-06CH11357

OSTI ID:: 1631858

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Issue 20; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 30 works

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References (102)

Improved Treatment of Ligands and Coupling Effects in Empirical Calculation and Rationalization of p K _a Values Søndergaard, Chresten R.; Olsson, Mats H. M.; Rostkowski, Michał Journal of Chemical Theory and Computation, Vol. 7, Issue 7 https://doi.org/10.1021/ct200133y	journal	June 2011
Constant pressure molecular dynamics for molecular systems Nosé, Shuichi; Klein, M. L. Molecular Physics, Vol. 50, Issue 5 https://doi.org/10.1080/00268978300102851	journal	December 1983
Ribulose Diphosphate Carboxylase regulates Soybean Photorespiration Ogren, William L.; Bowes, George Nature New Biology, Vol. 230, Issue 13 https://doi.org/10.1038/newbio230159a0	journal	March 1971
Crystal structure of tyrosine decarboxylase and identification of key residues involved in conformational swing and substrate binding Zhu, Haixia; Xu, Guochao; Zhang, Kai Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27779	journal	June 2016
Reaction of Dopa Decarboxylase with α-Methyldopa Leads to an Oxidative Deamination Producing 3,4-Dihydroxyphenylacetone, an Active Site Directed Affinity Label ^† Bertoldi, Mariarita; Dominici, Paola; Moore, Patrick S. Biochemistry, Vol. 37, Issue 18 https://doi.org/10.1021/bi9718898	journal	May 1998
An Aldol Switch Discovered in Stilbene Synthases Mediates Cyclization Specificity of Type III Polyketide Synthases Austin, Michael B.; Bowman, Marianne E.; Ferrer, Jean-Luc Chemistry & Biology, Vol. 11, Issue 9 https://doi.org/10.1016/j.chembiol.2004.05.024	journal	September 2004
Open conformation of human DOPA decarboxylase reveals the mechanism of PLP addition to Group II decarboxylases Giardina, G.; Montioli, R.; Gianni, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 51 https://doi.org/10.1073/pnas.1111456108	journal	December 2011
One thousand plant transcriptomes and the phylogenomics of green plants Nature, Vol. 574, Issue 7780, p. 679-685 https://doi.org/10.1038/s41586-019-1693-2	journal	October 2019
Plant Phenylacetaldehyde Synthase Is a Bifunctional Homotetrameric Enzyme That Catalyzes Phenylalanine Decarboxylation and Oxidation Kaminaga, Yasuhisa; Schnepp, Jennifer; Peel, Greg Journal of Biological Chemistry, Vol. 281, Issue 33 https://doi.org/10.1074/jbc.M602708200	journal	June 2006
Tryptophan decarboxylase from Catharanthus roseus cell suspension cultures: purification, molecular and kinetic data of the homogenous protein No�, W.; Mollenschott, C.; Berlin, J. Plant Molecular Biology, Vol. 3, Issue 5 https://doi.org/10.1007/BF00017782	journal	January 1984
Controlling reaction specificity in pyridoxal phosphate enzymes Toney, Michael D. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1814, Issue 11 https://doi.org/10.1016/j.bbapap.2011.05.019	journal	November 2011
Ornithine and glutamate decarboxylases catalyse an oxidative deamination of their α-methyl substrates Bertoldi, Mariarita; Carbone, Virginia; Voltattorni, Carla BORRI Biochemical Journal, Vol. 342, Issue 3 https://doi.org/10.1042/bj3420509	journal	September 1999
Biochemical and Structural Analysis of Substrate Promiscuity in Plant Mg2+-Dependent O-Methyltransferases Kopycki, Jakub G.; Rauh, Daniel; Chumanevich, Alexander A. Journal of Molecular Biology, Vol. 378, Issue 1 https://doi.org/10.1016/j.jmb.2008.02.019	journal	April 2008
The Shikimate Pathway and Aromatic Amino Acid Biosynthesis in Plants Maeda, Hiroshi; Dudareva, Natalia Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105439	journal	June 2012
Unleashing the Synthetic Power of Plant Oxygenases: From Mechanism to Application Mitchell, Andrew J.; Weng, Jing-Ke Plant Physiology, Vol. 179, Issue 3 https://doi.org/10.1104/pp.18.01223	journal	January 2019
Genomic Signatures of Specialized Metabolism in Plants Chae, L.; Kim, T.; Nilo-Poyanco, R. Science, Vol. 344, Issue 6183 https://doi.org/10.1126/science.1252076	journal	May 2014
Crystal Structure and Substrate Specificity of Drosophila 3,4-Dihydroxyphenylalanine Decarboxylase Han, Qian; Ding, Haizhen; Robinson, Howard PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008826	journal	January 2010
Structural investigation of heteroyohimbine alkaloid synthesis reveals active site elements that control stereoselectivity Stavrinides, Anna; Tatsis, Evangelos C.; Caputi, Lorenzo Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12116	journal	July 2016
Complete Pathway Elucidation and Heterologous Reconstitution of Rhodiola Salidroside Biosynthesis Torrens-Spence, Michael P.; Pluskal, Tomáš; Li, Fu-Shuang Molecular Plant, Vol. 11, Issue 1 https://doi.org/10.1016/j.molp.2017.12.007	journal	January 2018
Functionally Important Residues of Aromatic L-Amino Acid Decarboxylase Probed by Sequence Alignment and Site-Directed Mutagenesis Ishii, S.; Mizuguchi, H.; Nishino, J. Journal of Biochemistry, Vol. 120, Issue 2 https://doi.org/10.1093/oxfordjournals.jbchem.a021422	journal	August 1996
P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation Hess, Berk Journal of Chemical Theory and Computation, Vol. 4, Issue 1 https://doi.org/10.1021/ct700200b	journal	December 2007
Benzylisoquinoline Alkaloid Metabolism: A Century of Discovery and a Brave New World Hagel, Jillian M.; Facchini, Peter J. Plant and Cell Physiology, Vol. 54, Issue 5 https://doi.org/10.1093/pcp/pct020	journal	March 2013
Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds Mumberg, Dominik; Müller, Rolf; Funk, Martin Gene, Vol. 156, Issue 1 https://doi.org/10.1016/0378-1119(95)00037-7	journal	April 1995
Diverse functional evolution of serine decarboxylases: identification of two novel acetaldehyde synthases that uses hydrophobic amino acids as substrates Torrens-Spence, Michael P.; von Guggenberg, Renee; Lazear, Michael BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870-014-0247-x	journal	September 2014
ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins Gouet, P. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg556	journal	July 2003
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers Abraham, Mark James; Murtola, Teemu; Schulz, Roland SoftwareX, Vol. 1-2 https://doi.org/10.1016/j.softx.2015.06.001	journal	September 2015
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
Automation of the CHARMM General Force Field (CGenFF) I: Bond Perception and Atom Typing Vanommeslaeghe, K.; MacKerell, A. D. Journal of Chemical Information and Modeling, Vol. 52, Issue 12 https://doi.org/10.1021/ci300363c	journal	November 2012
CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields Vanommeslaeghe, K.; Hatcher, E.; Acharya, C. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21367	journal	January 2009
Investigation of a substrate-specifying residue within Papaver somniferum and Catharanthus roseus aromatic amino acid decarboxylases Torrens-Spence, Michael P.; Lazear, Michael; von Guggenberg, Renee Phytochemistry, Vol. 106 https://doi.org/10.1016/j.phytochem.2014.07.007	journal	October 2014
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
Substitution of Apolar Residues in the Active Site of Aspartate Aminotransferase by Histidine. Effects on Reaction and Substrate Specificity Vacca, Rosa Anna; Christen, Philipp; Malashkevich, Vladimir N. European Journal of Biochemistry, Vol. 227, Issue 1-2 https://doi.org/10.1111/j.1432-1033.1995.tb20413.x	journal	January 1995
Extension of the CHARMM general force field to sulfonyl-containing compounds and its utility in biomolecular simulations Yu, Wenbo; He, Xibing; Vanommeslaeghe, Kenno Journal of Computational Chemistry, Vol. 33, Issue 31 https://doi.org/10.1002/jcc.23067	journal	July 2012
The Decisive Step in Betaxanthin Biosynthesis Is a Spontaneous Reaction ¹ Schliemann, Willibald; Kobayashi, Naoko; Strack, Dieter Plant Physiology, Vol. 119, Issue 4 https://doi.org/10.1104/pp.119.4.1217	journal	April 1999
Rapid parameterization of small molecules using the force field toolkit Mayne, Christopher G.; Saam, Jan; Schulten, Klaus Journal of Computational Chemistry, Vol. 34, Issue 32 https://doi.org/10.1002/jcc.23422	journal	September 2013
PLUMED 2: New feathers for an old bird Tribello, Gareth A.; Bonomi, Massimiliano; Branduardi, Davide Computer Physics Communications, Vol. 185, Issue 2 https://doi.org/10.1016/j.cpc.2013.09.018	journal	February 2014
Aminotransferases: demonstration of homology and division into evolutionary subgroups Mehta, Perdeep K.; Hale, Terence I.; Christen, Philipp European Journal of Biochemistry, Vol. 214, Issue 2 https://doi.org/10.1111/j.1432-1033.1993.tb17953.x	journal	June 1993
Oxygenase side reactions of acetolactate synthase and other carbanion-forming enzymes Abell, Lynn M.; Schloss, John V. Biochemistry, Vol. 30, Issue 32 https://doi.org/10.1021/bi00246a002	journal	August 1991
Automation of the CHARMM General Force Field (CGenFF) II: Assignment of Bonded Parameters and Partial Atomic Charges Vanommeslaeghe, K.; Raman, E. Prabhu; MacKerell, A. D. Journal of Chemical Information and Modeling, Vol. 52, Issue 12 https://doi.org/10.1021/ci3003649	journal	November 2012
Structural Basis of Enzymatic ( S )-Norcoclaurine Biosynthesis Ilari, Andrea; Franceschini, Stefano; Bonamore, Alessandra Journal of Biological Chemistry, Vol. 284, Issue 2 https://doi.org/10.1074/jbc.M803738200	journal	November 2008
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical p K _a Predictions Olsson, Mats H. M.; Søndergaard, Chresten R.; Rostkowski, Michal Journal of Chemical Theory and Computation, Vol. 7, Issue 2 https://doi.org/10.1021/ct100578z	journal	December 2010
Rat liver aromatic L-amino acid decarboxylase: Spectroscopic and kinetic analysis of the coenzyme and reaction intermediates Hayashi, Hideyuki; Mizuguchi, Hiroyuki; Kagamiyama, Hiroyuki Biochemistry, Vol. 32, Issue 3 https://doi.org/10.1021/bi00054a011	journal	January 1993
Conformation and reaction specificity in pyridoxal phosphate enzymes. Dunathan, H. C. Proceedings of the National Academy of Sciences, Vol. 55, Issue 4 https://doi.org/10.1073/pnas.55.4.712	journal	April 1966
Multiple Sequence Alignment Using ClustalW and ClustalX Thompson, Julie D.; Gibson, Toby. J.; Higgins, Des G. Current Protocols in Bioinformatics, Vol. 00, Issue 1 https://doi.org/10.1002/0471250953.bi0203s00	journal	August 2002
Biochemical Evaluation of the Decarboxylation and Decarboxylation-Deamination Activities of Plant Aromatic Amino Acid Decarboxylases Torrens-Spence, Michael P.; Liu, Pingyang; Ding, Haizhen Journal of Biological Chemistry, Vol. 288, Issue 4 https://doi.org/10.1074/jbc.M112.401752	journal	November 2012
Canonical sampling through velocity rescaling Bussi, Giovanni; Donadio, Davide; Parrinello, Michele The Journal of Chemical Physics, Vol. 126, Issue 1 https://doi.org/10.1063/1.2408420	journal	January 2007
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Biochemical evaluation of a parsley tyrosine decarboxylase results in a novel 4-hydroxyphenylacetaldehyde synthase enzyme Torrens-Spence, Michael P.; Gillaspy, Glenda; Zhao, Bingyu Biochemical and Biophysical Research Communications, Vol. 418, Issue 2 https://doi.org/10.1016/j.bbrc.2011.12.124	journal	February 2012
Composition of Australian Honey Extractives. 1. Norisoprenoids, Monoterpenes, and Other Natural Volatiles from Blue Gum (Eucalyptusleucoxylon)and Yellow Box (Eucalyptus melliodora)Honeys D'Arcy, Bruce R.; Rintoul, Gavin B.; Rowland, Catherine Y. Journal of Agricultural and Food Chemistry, Vol. 45, Issue 5 https://doi.org/10.1021/jf960625+	journal	May 1997
Chemical Composition and Antimicrobial Activity of the Essential Oil from Microlicia crenulata Pereira, Maria do Carmo; Nelson, David Lee; Stoianoff, Maria Aparecida Resende Journal of Essential Oil Bearing Plants, Vol. 18, Issue 1 https://doi.org/10.1080/0972060X.2014.935055	journal	January 2015
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ ₁ and χ ₂ Dihedral Angles Best, Robert B.; Zhu, Xiao; Shim, Jihyun Journal of Chemical Theory and Computation, Vol. 8, Issue 9 https://doi.org/10.1021/ct300400x	journal	August 2012
Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Kabsch, Wolfgang; Sander, Christian Biopolymers, Vol. 22, Issue 12 https://doi.org/10.1002/bip.360221211	journal	December 1983
Enzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates Huang, R.; Hippauf, F.; Rohrbeck, D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 8 https://doi.org/10.1073/pnas.1019605109	journal	February 2012
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L	journal	September 1997
A Highly Characterized Yeast Toolkit for Modular, Multipart Assembly Lee, Michael E.; DeLoache, William C.; Cervantes, Bernardo ACS Synthetic Biology, Vol. 4, Issue 9 https://doi.org/10.1021/sb500366v	journal	April 2015
Role of aromatic aldehyde synthase in wounding/herbivory response and flower scent production in different Arabidopsis ecotypes: Phenylacetaldehyde biosynthesis in A. thaliana Gutensohn, Michael; Klempien, Antje; Kaminaga, Yasuhisa The Plant Journal, Vol. 66, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04515.x	journal	March 2011
The Remarkable Pliability and Promiscuity of Specialized Metabolism Weng, J. - K.; Noel, J. P. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0 https://doi.org/10.1101/sqb.2012.77.014787	journal	January 2012
Evolution of chalcone isomerase from a noncatalytic ancestor Kaltenbach, Miriam; Burke, Jason R.; Dindo, Mirco Nature Chemical Biology, Vol. 14, Issue 6 https://doi.org/10.1038/s41589-018-0042-3	journal	April 2018
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Chemical Composition of Turkish Myrtle Oil Özek, T.; Demirci, B.; Baser, K. H. C. Journal of Essential Oil Research, Vol. 12, Issue 5 https://doi.org/10.1080/10412905.2000.9712154	journal	September 2000
Designed divergent evolution of enzyme function Yoshikuni, Yasuo; Ferrin, Thomas E.; Keasling, Jay D. Nature, Vol. 440, Issue 7087 https://doi.org/10.1038/nature04607	journal	February 2006
3,4-Dihydroxyphenylacetaldehyde synthase and cuticle formation in insects Liao, Chenghong; Upadhyay, Archana; Liang, Jing Developmental & Comparative Immunology, Vol. 83 https://doi.org/10.1016/j.dci.2017.11.007	journal	June 2018
Biochemical identification of residues that discriminate between 3,4-dihydroxyphenylalanine decarboxylase and 3,4-dihydroxyphenylacetaldehyde synthase-mediated reactions Liang, Jing; Han, Qian; Ding, Haizhen Insect Biochemistry and Molecular Biology, Vol. 91 https://doi.org/10.1016/j.ibmb.2017.10.001	journal	December 2017
The Rise of Chemodiversity in Plants Weng, Jing-Ke; Philippe, Ryan N.; Noel, Joseph P. Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1217411	journal	June 2012
MOLREP an Automated Program for Molecular Replacement Vagin, A.; Teplyakov, A. Journal of Applied Crystallography, Vol. 30, Issue 6, p. 1022-1025 https://doi.org/10.1107/S0021889897006766	journal	December 1997
Production of 2-Phenylethanol in Roses as the Dominant Floral Scent Compound from L -Phenylalanine by Two Key Enzymes, a PLP-Dependent Decarboxylase and a Phenylacetaldehyde Reductase Sakai, Miwa; Hirata, Hiroshi; Sayama, Hironori Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 10 https://doi.org/10.1271/bbb.70090	journal	October 2007
Mechanism-based tuning of insect 3,4-dihydroxyphenylacetaldehyde synthase for synthetic bioproduction of benzylisoquinoline alkaloids Vavricka, Christopher J.; Yoshida, Takanobu; Kuriya, Yuki Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09610-2	journal	May 2019
Escaping free-energy minima Laio, A.; Parrinello, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.202427399	journal	September 2002
Structural determinants of reductive terpene cyclization in iridoid biosynthesis Kries, Hajo; Caputi, Lorenzo; Stevenson, Clare E. M. Nature Chemical Biology, Vol. 12, Issue 1 https://doi.org/10.1038/nchembio.1955	journal	November 2015
Structure, evolution and action of vitamin B6-dependent enzymes Jansonius, Johan N. Current Opinion in Structural Biology, Vol. 8, Issue 6 https://doi.org/10.1016/S0959-440X(98)80096-1	journal	December 1998
Monoamine Biosynthesis via a Noncanonical Calcium-Activatable Aromatic Amino Acid Decarboxylase in Psilocybin Mushroom Torrens-Spence, Michael Patrick; Liu, Chun-Ting; Pluskal, Tomáš ACS Chemical Biology, Vol. 13, Issue 12 https://doi.org/10.1021/acschembio.8b00821	journal	November 2018
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Multiple evolutionary origin of pyridoxal-5'-phosphate-dependent amino acid decarboxylases Sandmeier, Erika; Hale, Terence I.; Christen, Philipp European Journal of Biochemistry, Vol. 221, Issue 3 https://doi.org/10.1111/j.1432-1033.1994.tb18816.x	journal	May 1994
Differential and tissue-specific expression of a gene family for tyrosine/dopa decarboxylase in opium poppy. Facchini, P. J.; De Luca, V. Journal of Biological Chemistry, Vol. 269, Issue 43 https://doi.org/10.1016/S0021-9258(18)47073-1	journal	October 1994
Chemical modification of pig kidney 3,4-dihydroxyphenylalanine decarboxylase with diethyl pyrocarbonate. Evidence for an essential histidyl residue. Dominici, P.; Tancini, B.; Borri Voltattorni, C. Journal of Biological Chemistry, Vol. 260, Issue 19 https://doi.org/10.1016/S0021-9258(19)85125-6	journal	September 1985
Characterization of rice tryptophan decarboxylases and their direct involvement in serotonin biosynthesis in transgenic rice Kang, Sei; Kang, Kiyoon; Lee, Kyungjin Planta, Vol. 227, Issue 1 https://doi.org/10.1007/s00425-007-0614-z	journal	September 2007
Induction of serotonin biosynthesis is uncoupled from the coordinated induction of tryptophan biosynthesis in pepper fruits (Capsicum annuum) upon pathogen infection Park, Sangkyu; Kang, Kiyoon; Lee, Kyungjin Planta, Vol. 230, Issue 6 https://doi.org/10.1007/s00425-009-1015-2	journal	September 2009
Improving the specificity of organophosphorus hydrolase to acephate by mutagenesis at its binding site: a computational study Badakhshan, Reza; Mohammadi, Mozafar; Farnoosh, Gholamreza Journal of Molecular Modeling, Vol. 27, Issue 6 https://doi.org/10.1007/s00894-021-04749-6	journal	May 2021
Gene expression and characterization of a stress-induced tyrosine decarboxylase from Arabidopsis thaliana Lehmann, Thomas; Pollmann, Stephan FEBS Letters, Vol. 583, Issue 12 https://doi.org/10.1016/j.febslet.2009.05.017	journal	May 2009
A Combined Quantum Mechanical and Molecular Mechanical Study of the Reaction Mechanism and α-Amino Acidity in Alanine Racemase Major, Dan Thomas; Gao, Jiali Journal of the American Chemical Society, Vol. 128, Issue 50 https://doi.org/10.1021/ja066334r	journal	December 2006
NMR Studies of Protonation and Hydrogen Bond States of Internal Aldimines of Pyridoxal 5′-Phosphate Acid–Base in Alanine Racemase, Aspartate Aminotransferase, and Poly- l -lysine Chan-Huot, Monique; Dos, Alexandra; Zander, Reinhard Journal of the American Chemical Society, Vol. 135, Issue 48 https://doi.org/10.1021/ja408988z	journal	November 2013
Protonation States of the Tryptophan Synthase Internal Aldimine Active Site from Solid-State NMR Spectroscopy: Direct Observation of the Protonated Schiff Base Linkage to Pyridoxal-5′-Phosphate Caulkins, Bethany G.; Bastin, Baback; Yang, Chen Journal of the American Chemical Society, Vol. 136, Issue 37 https://doi.org/10.1021/ja506267d	journal	September 2014
¹⁵ N Nuclear Magnetic Resonance Studies of Acid−Base Properties of Pyridoxal-5‘-Phosphate Aldimines in Aqueous Solution Sharif, Shasad; Huot, Monique Chan; Tolstoy, Peter M. The Journal of Physical Chemistry B, Vol. 111, Issue 15 https://doi.org/10.1021/jp067334g	journal	April 2007
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
Rational identification and characterisation of peptide ligands for targeting polysialic acid Shastry, Divya G.; Irudayanathan, Flaviyan Jerome; Williams, Asher Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-64088-z	journal	May 2020
A multi-omic characterization of temperature stress in a halotolerant Scenedesmus strain for algal biotechnology Calhoun, Sara; Bell, Tisza Ann Szeremy; Dahlin, Lukas R. Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01859-y	journal	March 2021
Ornithine and glutamate decarboxylases catalyse an oxidative deamination of their α-methyl substrates Bertoldi, Mariarita; Carbone, Virginia; Borri Voltattorni, Carla Biochemical Journal, Vol. 342, Issue 3 https://doi.org/10.1042/0264-6021:3420509	journal	September 1999
Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases. De Luca, V.; Marineau, C.; Brisson, N. Proceedings of the National Academy of Sciences, Vol. 86, Issue 8 https://doi.org/10.1073/pnas.86.8.2582	journal	April 1989
Mutation of Tyrosine 332 to Phenylalanine Converts Dopa Decarboxylase into a Decarboxylation-dependent Oxidative Deaminase Bertoldi, Mariarita; Gonsalvi, Marco; Contestabile, Roberto Journal of Biological Chemistry, Vol. 277, Issue 39 https://doi.org/10.1074/jbc.m204867200	journal	September 2002
Automatic generation of protein structure cartoons with Pro-origami Stivala, A.; Wybrow, M.; Wirth, A. Bioinformatics, Vol. 27, Issue 23 https://doi.org/10.1093/bioinformatics/btr575	journal	October 2011
Camptothecin Biosynthetic Genes in Hairy Roots of Ophiorrhiza pumila: Cloning, Characterization and Differential Expression in Tissues and by Stress Compounds Yamazaki, Yasuyo; Sudo, Hiroshi; Yamazaki, Mami Plant and Cell Physiology, Vol. 44, Issue 4 https://doi.org/10.1093/pcp/pcg051	journal	April 2003
Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar Günther, Jan; Lackus, Nathalie D.; Schmidt, Axel Plant Physiology, Vol. 180, Issue 2 https://doi.org/10.1104/pp.19.00059	journal	March 2019
Pyridoxal Phosphate Enzymes: Mechanistic, Structural, and Evolutionary Considerations Eliot, Andrew C.; Kirsch, Jack F. Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.074021	journal	June 2004
Data access for the 1,000 Plants (1KP) project Matasci, Naim; Hung, Ling-Hong; Yan, Zhixiang GigaScience, Vol. 3, Issue 1 https://doi.org/10.1186/2047-217X-3-17	journal	October 2014
From L-Dopa to Dihydroxyphenylacetaldehyde: A Toxic Biochemical Pathway Plays a Vital Physiological Function in Insects Vavricka, Christopher; Han, Qian; Huang, Yongping PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016124	journal	January 2011
Evaluation of Brachypodium distachyon L-Tyrosine Decarboxylase Using L-Tyrosine Over-Producing Saccharomyces cerevisiae Noda, Shuhei; Shirai, Tomokazu; Mochida, Keiichi PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0125488	journal	May 2015
Data access for the 1,000 Plants (1KP) project Matasci, Naim; Hung, Ling-Hong; Yan, Zhixiang BioMed Central https://doi.org/10.14288/1.0132648	text	January 2014

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General and specialized tyrosine metabolism pathways in plants Xu, Jing-Jing; Fang, Xin; Li, Chen-Yi aBIOTECH https://doi.org/10.1007/s42994-019-00006-w	journal	September 2019
Untargeted and Targeted Metabolomics and Tryptophan Decarboxylase In Vivo Characterization Provide Novel Insight on the Development of Kiwifruits (Actinidia deliciosa) Commisso, Mauro; Negri, Stefano; Bianconi, Martino International Journal of Molecular Sciences, Vol. 20, Issue 4 https://doi.org/10.3390/ijms20040897	journal	February 2019

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