bioRxiv Science⌕ Search

Biology subjects

Weng, J.-K.

Publications and source records attributed to Weng, J.-K..

18 recordsLinked to original sources

Elucidating enzyme-substrate specificity through co-folding foundation model

Enzymatic catalysis relies on precise structural and chemical complementarity, yet systematically mapping enzyme-substrate interactions remains a critical bottleneck. While structure-aware methods have advanced functional annotation, their reliance on predefined binding pockets and rigid-body docking fails to capture the ligand-induced conformational changes essential for catalytic turnover. Here we introduce Boltz2ESI, an end-to-end framework that predicts enzyme-substrate interactions by leveraging structural knowledge learned by a biomolecular foundation model. Through native co-folding, the framework inherently captures active-site plasticity without requiring predefined pocket annotations. Integrating these learned biophysical priors with global evolutionary context and geometric molecular descriptors, Boltz2ESI consistently outperforms state-of-the-art sequence-based and rigid-docking approaches. Extensive validation demonstrates that the framework accurately discriminates tight sub-family specificities, enabling effective candidate prioritization for biosynthetic pathway elucidation, as demonstrated on the withanolide pathway. Ultimately, this structure-dynamic approach establishes an actionable foundation for accelerating rational biocatalyst discovery and large-scale pathway de-orphaning.

bioinformatics↗

Neural Spectral Prediction for Structure Elucidation with Tandem Mass Spectrometry

Structural elucidation using untargeted tandem mass spectrometry (MS/MS) has played a critical role in advancing scientific discovery [1, 2]. However, differentiating molecular fragmentation patterns between isobaric structures remains a prominent challenge in metabolomics [3-10], drug discovery [11-13], and reaction screening [14-17], presenting a significant barrier to the cost-effective and rapid identification of unknown molecular structures. Here, we present a geometric deep learning model, ICEBERG, that simulates high-energy collision-induced dissociation in mass spectrometry to generate chemically plausible fragments and their relative intensities with awareness of collision energies and polarities. We utilize ICEBERG predictions to facilitate structure elucidation by ranking a set of candidate structures based on the similarity between their predicted in silico MS/MS spectra and an experimental MS/MS spectrum of interest. This integrated elucidation pipeline enables state-of-the-art performance in compound annotation, with 40% top-1 accuracy on the NIST20 [M+H]+ adduct subset and with 92% of correct structures appearing in the top ten predictions in the same dataset. It achieves 46% top-1 and 86% top-10 accuracies when tested on the open-access MassSpecGym benchmark, and outperforms SIRIUS on a recently released test set with previously uncharacterized structures. We demonstrate several real-world case studies, including identifying clinical biomarkers of depression and tuberculous meningitis, annotating an aqueous abiotic degradation product of the pesticide thiophanate methyl, disambiguating isobaric products in pooled reaction screening, and annotating biosynthetic pathways in Withania somnifera. Overall, this deep learning-based paradigm for structural elucidation enables rapid molecular annotation from complex mixtures, driving discoveries across diverse scientific domains.

bioinformatics↗

Elucidation of gene clusters underlying withanolide biosynthesis in ashwagandha through yeast metabolic engineering

Withanolides are medicinally relevant steroidal lactones produced by Withania somnifera (ashwagandha) amongst other Solanaceae family plants. However, the biosynthetic pathway to withanolides is largely unknown, preventing scale-up and hindering pharmaceutical applications. We sequenced the genome of W. somnifera and identified two biosynthetic gene clusters exhibiting a segmented tissue-specific expression pattern. We characterized the cluster enzymes through stepwise pathway reconstitution in yeast and transient expression in Nicotiana benthamiana, leading to the identification of three cytochrome P450s (CYP87G1, CYP88C7, and CYP749B2) and a short-chain dehydrogenase that produce a lactone ring- containing intermediate when co-expressed. A fourth cytochrome P450 (CYP88C10) and a sulfotransferase convert this into an intermediate with the characteristic withanolide A-ring structure, featuring a C1 ketone and C2-C3 unsaturation. The discovery of the sulfotransferase as a core pathway enzyme challenges the conventional paradigm of sulfotransferases as tailoring enzymes. These insights pave the way for an efficient biomanufacturing process for withanolides and future development of withanolide-derived drugs.

biochemistry↗

Tracing the stepwise Darwinian evolution of a plant halogenase

Halogenation chemistry is rare in plant metabolism, with the chloroalkaloid acutumine produced by Menispermaceae species being the only well characterized example, involving a specialized dechloroacutumine halogenase (DAH) from the iron(II)- and 2-oxoglutarate-dependent dioxygenase (2ODD) superfamily. While DAH is presumed to have evolved from an ancestral 2ODD enzyme, the broader question of how new enzymes arise through Darwinian processes, such as the birth of DAH in Menispermaceae, remains a fundamental challenge in understanding metabolic evolution. Here, we investigate DAHs evolutionary trajectory using the chromosomal-level genome assembly of Menispermum canadense. By analyzing the genomic context of DAH in M. canadense and syntenic regions in related plants, we show that DAH evolved through tandem duplication of an ancestral flavonol synthase (FLS) gene, followed by a series of neofunctionalization and gene loss events. Through structural modeling, molecular dynamics simulations, and site-directed mutagenesis, we identify residue changes enabling the transition from FLS to DAH. This functional switch required traversing a complex evolutionary landscape where adaptive peaks were separated by deep fitness valleys. Our work illustrates how new enzymatic functions can arise through lineage-specific evolutionary pathways that gradually reshape the active site architecture through permissive mutations, ultimately enabling mechanism-switching mutations that establish novel catalytic activities.

biochemistry↗

The emergence and loss of cyclic peptides in Nicotiana illuminate dynamics and mechanisms of plant metabolic evolution

Specialized metabolism plays a central role in how plants cope with both biotic and abiotic stresses in order to survive and reproduce within dynamic and challenging environments. One recently circumscribed class of plant-specific, ribosomally synthesized and post-translationally modified peptides are the burpitides, which are characterized by the installation of distinct sidechain macrocycles by enzymes known as burpitide cyclases. While they are found across many plant families and exhibit diverse bioactivities, little is known about their evolution or how new variants arise. Here we present the discovery of a new burpitide cyclase, resurrected from a defunct pseudogene from the model organism Nicotiana attenuata, the coyote tobacco. By repairing the pseudogene{Psi} NatBURP2 and expressing it heterologously in Nicotiana benthamiana, we successfully reconstituted its original enzymatic activity. As an autocatalytic peptide cyclase, it installs a unique C-C bond between the tyrosine side chain and a specific backbone a-carbon of a heptapeptide core motif, resulting in the burpitide dubbed "nanamin." Despite its pseudogenization in N. attenuata, we found that the closely related species, N. clevelandii, retains the wild-type gene and produces nanamins. Phylogenetic analyses and targeted mutagenesis experiments reveal that this chemotype must have evolved from the duplication and neofunctionalization of a more promiscuous ancestral gene. This work highlights how novel peptide chemotypes may rapidly emerge and disappear in plants, while expanding the molecular toolkit for engineering novel peptides with applications in agriculture and drug discovery. SignificanceWhile RiPPs represent a major source of antibiotics and bioactive compounds, much research has focused on microbial sources even as plant RiPPs go understudied. Here, we resurrect an extinct peptide cyclase from the coyote tobacco through analysis of its functional relatives in other species. This newly identified cyclase installs a novel carbon-carbon macrocycle into heptapeptides, expanding the diversity of plant-derived cyclic peptides. By interconverting two distinct cyclases through targeted mutations, we illuminate how these enzymes evolve new functions. This work highlights the evolutionary dynamics of plant peptide natural products and their potential applications in drug discovery and biotech crop development, while illustrating how genomic archaeology can reveal lost biosynthetic capabilities.

biochemistry↗

A genetically encoded fluorescent reporter for polyamines

Polyamines are abundant and evolutionarily conserved metabolites that are essential for life. Dietary polyamine supplementation extends life-span and health-span. Dysregulation of polyamine homeostasis is linked to Parkinsons disease and cancer, driving interest in therapeutically targeting this pathway. However, measuring cellular polyamine levels, which vary across cell types and states, remains challenging. We introduce a first-in-class genetically encoded polyamine reporter for real-time measurement of polyamine concentrations in single living cells. This reporter utilizes the polyamine-responsive ribosomal frameshift motif from the OAZ1 gene. We demonstrate broad applicability of this approach and reveal dynamic changes in polyamine levels in response to genetic and pharmacological perturbations. Using this reporter, we conducted a genome-wide CRISPR screen and uncovered an unexpected link between mitochondrial respiration and polyamine import, which are both risk factors for Parkinsons disease. By offering a new lens to examine polyamine biology, this reporter may advance our understanding of these ubiquitous metabolites and accelerate therapy development.

cell biology↗

Emergence of a proton exchange-based isomerization and lactonization mechanism in the plant coumarin synthase COSY

Plants contain rapidly evolving specialized metabolic enzymes to support the synthesis of a myriad of functionally diverse natural products. In the case of coumarin biosynthesis, a BAHD acyltransferase-family enzyme COSY was recently discovered in Arabidopsis that catalyzes coumarin formation from o-hydroxylated trans-hydroxycinnamoyl-CoA substrates. COSY is the first and only BAHD enzyme known to date that catalyzes an intramolecular acyl transfer reaction. Here we combine structural, biochemical, and computational approaches to investigate the mechanistic basis for the unique coumarin synthase activity of COSY. Comparative analyses of crystal structures of Arabidopsis thaliana COSY relative to other BAHD proteins reveal that COSY possesses an unconventional active-site configuration adapted to its specialized activity. Through deuterium exchange experiments, we discover a unique proton exchange mechanism at the -carbon of the o-hydroxylated trans-hydroxycinnamoyl-CoA substrates during the catalytic cycle of COSY. Mutagenesis studies and quantum mechanical cluster modeling further support that this mechanism is key to COSYs ability to lower the activation energy of the trans-to-cis isomerization of the hydroxycinnamoyl-CoA substrates, a critical rate-limiting step leading to coumarin production. This study unveils the emergence of an unconventional catalytic mechanism mediated by a BAHD-family enzyme, and sheds light on the potential evolutionary origin of COSY and its recruitment to the evolutionarily new coumarin biosynthetic pathway in eudicots.

biochemistry↗

Mechanistic basis for the emergence of EPS1 as a catalyst in plant salicylic acid biosynthesis

Unique to plants in the Brassicaceae family, the production of the plant defense hormone salicylic acid (SA) from isochorismate is accelerated by an evolutionarily young isochorismoyl-glutamate pyruvoyl-glutamate lyase, EPS1, which belongs to the BAHD acyltransferase protein family. Here, we report the crystal structures of apo and substrate-analog-bound EPS1 from Arabidopsis thaliana. Assisted by microsecond molecular dynamics simulations, we uncover a unique pericyclic rearrangement lyase mechanism facilitated by the active site of EPS1. We reconstitute the isochorismate-derived pathway of SA biosynthesis in Saccharomyces cerevisiae, which serves as an in vivo platform that helps identify active-site residues critical for EPS1 activity. This study describes the birth of a new catalyst in plant phytohormone biosynthesis by reconfiguring the ancestral active site of a progenitor enzyme to catalyze alternative reaction. One sentence summaryBy reconfiguring the active site of a progenitor acyltransferase-fold, EPS1 acquired the unique, evolutionarily new lyase activity that accelerates phytohormone salicylic acid production in Brassicaceae plants.

biochemistry↗

Laboratory culture of the California Sea Firefly Vargula tsujii (Ostracoda: Cypridinidae): Developing a model system for the evolution of marine bioluminescence

Bioluminescence, or the production of light by living organisms via chemical reaction, is widespread across Metazoa. Culture of bioluminescent organisms from diverse taxonomic groups is important for determining the biosynthetic pathways of bioluminescent substrates, which may lead to new tools for biotechnology and biomedicine. Some bioluminescent groups may be cultured, including some cnidarians, ctenophores, and brittle stars, but those use luminescent substrates (luciferins) obtained from their diets, and therefore are not informative for determination of the biosynthethic pathways of the luciferins. Other groups, including terrestrial fireflies, do synthesize their own luciferin, but culturing them is difficult, and the biosynthetic pathway for firefly luciferin remains unclear. An additional independent origin of endogenous bioluminescence is found within ostracods from the family Cypridinidae, which use their luminescence for defense and, in Caribbean species, for courtship displays. Here, we report the first complete life cycle of a luminous ostracod (Vargula tsujii Kornicker & Baker, 1977, the California Sea Firefly) in the laboratory. We also describe the late-stage embryogenesis of Vargula tsujii and discuss the size classes of instar development. We find embryogenesis in V. tsujii ranges from 25-38 days, and this species appears to have five instar stages, consistent with ontogeny in other cypridinid lineages. We estimate a complete life cycle at 3-4 months. We also present the first complete mitochondrial genome for Vargula tsujii. Bringing a luminous ostracod into laboratory culture sets the stage for many potential avenues of study, including learning the biosynthetic pathway of cypridinid luciferin and genomic manipulation of an autogenic bioluminescent system.

developmental biology↗

PBS3 and EPS1 complete salicylic acid biosynthesis from isochorismate in Arabidopsis

Salicylic acid (SA) is an important phytohormone mediating both local and systemic defense responses in plants. Despite over half a century of research, how plants biosynthesize SA remains unresolved. In Arabidopsis, a major part of SA is derived from isochorismate, a key intermediate produced by the isochorismate synthase (ICS), which is reminiscent of SA biosynthesis in bacteria. Whereas bacteria employ an isochorismate pyruvate lyase (IPL) that catalyzes the turnover of isochorismate to pyruvate and SA, plants do not contain an IPL ortholog and generate SA from isochorismate through an unknown mechanism. Combining genetic and biochemical approaches, we delineated the SA biosynthetic pathway downstream of isochorismate in Arabidopsis. We show that PBS3, a GH3 acyl adenylase-family enzyme important for SA accumulation, catalyzes ATP- and Mg2+-dependent conjugation of L-glutamate primarily to the 8-carboxyl of isochorismate and yields the key SA biosynthetic intermediate isochorismoyl-glutamate A. Moreover, EPS1, a BAHD acyltransferase-family protein with previously implicated role in SA accumulation upon pathogen attack, harbors a noncanonical active site and an unprecedented isochorismoyl-glutamate A pyruvoyl-glutamate lyase (IPGL) activity that produces SA from the isochorismoyl-glutamate A substrate. Together, PBS3 and EPS1 form a two-step metabolic pathway to produce SA from isochorismate in Arabidopsis, which is distinct from how SA is biosynthesized in bacteria. This study closes a major knowledge gap in plant SA metabolism and would help develop new strategies for engineering disease resistance in crop plants.

plant biology↗

Production of nonnatural straight chain amino acid 6-aminocaproate via an artificial recursive carbon-chain-extension cycle

Bioplastics produced from microbial source are promising green alternatives to traditional petrochemical-derived plastics. Nonnatural straight-chain amino acids, especially 5-aminovalerate, 6-aminocaproate and 7-aminoheptanoate are potential monomers for the synthesis of polymeric bioplastics as their primary amine and carboxylic acid are ideal functional groups for polymerization. Previous pathways for 5-aminovalerate and 6-aminocaproate biosynthesis in microorganisms are derived from L-lysine catabolism and citric acid cycle, respectively. Here, we show the construction of an artificial iterative carbon-chain-extension cycle in Escherichia coli for simultaneous production of a series of nonnatural amino acids with varying chain length. Overexpression of L-lysine -oxidase in E. coli yields 2-keto-6-aminocaproate as a non-native substrate for the artificial iterative carbon-chain-extension cycle. The chain-extended -ketoacid is subsequently decarboxylated and oxidized by an -ketoacid decarboxylase and an aldehyde dehydrogenase, respectively, to yield the nonnatural straight-chain amino acid products. The engineered system demonstrated simultaneous in vitro production of 99.16 mg/L of 5-aminovalerate, 46.96 mg/L of 6-aminocaproate and 4.78 mg/L of 7-aminoheptanoate after 8 hours of enzyme catalysis starting from 2-keto-6-aminocaproate as the substrate. Furthermore, simultaneous production of 2.15 g/L of 5-aminovalerate, 24.12 mg/L of 6-aminocaproate and 4.74 mg/L of 7-aminoheptanoate was achieved in engineered E. coli. This work illustrates a promising metabolic-engineering strategy to access other medium-chain organic acids with -NH2,-SCH3, -SOCH3, -SH, -COOH, -COH, or -OH functional groups through carbon-chain-elongation chemistry.

synthetic biology↗

Mechanistic basis for the evolution of chalcone synthase catalytic cysteine reactivity in land plants

Flavonoids are important polyphenolic natural products, ubiquitous in land plants, that play diverse functions in plants survival in their ecological niches, including UV protection, pigmentation for attracting pollinators, symbiotic nitrogen fixation, and defense against herbivores. Chalcone synthase (CHS) catalyzes the first committed step in plant flavonoid biosynthesis and is highly conserved in all land plants. In several previously reported crystal structures of flowering plant CHSs, the catalytic cysteine is oxidized to sulfinic acid, indicating enhanced nucleophilicity in this residue associated with its increased susceptibility to oxidation. In this study, we report a set of new crystal structures of CHSs representing all five major lineages of land plants. We reveal that the structures of CHS from a lycophyte and a moss species preserve the catalytic cysteine in a reduced state, in contrast to the cysteine sulfinic acid seen in all euphyllophyte CHS structures. In vivo complementation, in vitro biochemical and mutagenesis analyses, as well as molecular dynamics simulations identify a set of residues that differ between basal-plant and euphyllophyte CHSs and modulate catalytic cysteine reactivity. We propose that the CHS active-site environment has evolved in euphyllophytes to further enhance the nucleophilicity of the catalytic cysteine since the divergence of euphyllophytes from other vascular plant lineages 400 million years ago. These changes in CHS could have contributed to the diversification of flavonoid biosynthesis in euphyllophytes, which in turn contributed to their dominance in terrestrial ecosystems.

biochemistry↗

The molecular structure of plant sporopollenin

Sporopollenin is a ubiquitous and extremely chemically inert biopolymer that constitutes the outer wall of all land-plant spores and pollen grains. Sporopollenin protects the vulnerable plant gametes against a wide range of environmental assaults, and is considered as a prerequisite for the migration of early plants onto land. Despite its importance, the chemical structure of plant sporopollenin has remained elusive. Using a newly developed thioacidolysis degradative method together with state-of-the-art solid-state NMR techniques, we determined the detailed molecular structure of pine sporopollenin. We show that pine sporopollenin is primarily composed of aliphatic-polyketide-derived polyvinyl alcohol units and 7-O-p-coumaroylated C16 aliphatic units, crosslinked through a distinctive m-dioxane moiety featuring an acetal. Naringenin was also identified as a minor component of pine sporopollenin. This discovery answers the long-standing question about the chemical makeup of plant sporopollenin, laying the foundation for future investigations of sporopollenin biosynthesis and for design of new biomimetic polymers with desirable inert properties.

biochemistry↗

Structural basis for independent origins of new catalytic machineries in plant AAAD proteins

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. Here, 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. SignificancePlants biosynthesize their own proteinogenic aromatic L-amino acids, namely L-phenylalanine, L-tyrosine and L-tryptophan, not only for building proteins but also for the production of a plethora of aromatic-amino-acid-derived natural products. Pyridoxal 5-phosphate (PLP)-dependent aromatic L-amino acid decarboxylase (AAAD) family enzymes play important roles in channeling various aromatic L-amino acids into diverse downstream specialized metabolic pathways. Through comparative structural analysis of four functionally divergent plant AAAD proteins together with biochemical characterization and molecular dynamics simulations, we reveal the structural and mechanistic basis for the rich divergent and convergent evolutionary development within the plant AAAD family. Knowledge learned from this study aids our ability to engineer high-value aromatic-L-amino-acid-derived natural product biosynthesis in heterologous chassis organisms.

biochemistry↗

PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during Arabidopsis anther development

Pollen and microspore development is an essential step in the life cycle of all land plants that generate male gametes. Within flowering plants, pollen development occurs inside of the anther. Here, we report the identification of two class III peroxidase-encoding genes, PRX9 and PRX40, that are genetically redundant and essential for proper anther and pollen development in Arabidopsis thaliana. Arabidopsis double mutants devoid of functional PRX9 and PRX40 are male-sterile. The mutant anthers display swollen, hypertrophic tapetal cells and pollen grains, suggesting disrupted cell wall integrity. These phenotypes ultimately lead to nearly 100%-penetrant pollen degeneration upon anther maturation. Using immunochemical and biochemical approaches, we show that PRX9 and PRX40 are likely extensin peroxidases that contribute to the establishment of tapetal cell wall integrity during anther development. This work identifies PRX9 and PRX40 as the first extensin peroxidases to be described in Arabidopsis and highlights the importance of extensin cross-linking during plant development.

plant biology↗

The biosynthetic origin of psychoactive kavalactones in kava

For millennia, humans have used plants for medicinal purposes. However, our limited understanding of plant biochemistry hinders the translation of such ancient wisdom into modern pharmaceuticals1. Kava (Piper methysticum) is a medicinal plant native to the Polynesian islands with anxiolytic and analgesic properties supported by over 3,000 years of traditional use as well as numerous recent clinical trials2-5. The main psychoactive principles of kava, kavalactones, are a unique class of polyketide natural products known to interact with central nervous system through mechanisms distinct from those of the prescription psychiatric drugs benzodiazepines and opioids6,7. Here we report de novo elucidation of the biosynthetic pathway of kavalactones, consisting of seven specialized metabolic enzymes. Based on phylogenetic and crystallographic analyses, we highlight the emergence of two paralogous styrylpyrone synthases, both of which have neofunctionalized from an ancestral chalcone synthase to catalyze the formation of the kavalactone scaffold. Structurally diverse kavalactones are then biosynthesized by subsequent regio- and stereo-specific tailoring enzymes. We demonstrate the feasibility of engineering heterologous production of kavalactones and their derivatives in bacterial, yeast, and plant hosts, thus opening an avenue towards the development of new psychiatric therapeutics for anxiety disorders, which affect over 260 million people globally8.

plant biology↗

Firefly genomes illuminate the origin and evolution of bioluminescence

Fireflies are among the best-studied of the bioluminescent organisms. Despite longterm interest in the biochemistry, neurobiology, and evolution of firefly flash signals and the widespread biotechnological applications of firefly luciferase, only a limited set of genes related to this complex trait have been described. To investigate the genetic basis of firefly bioluminescence, we generated a high-quality reference genome for the Big Dipper firefly Photinus pyralis, from which the first laboratory luciferase was cloned, using long-read (PacBio), short-read (Illumina), and Hi-C sequencing technologies. To facilitate comparative genomics, we also generated short-read genome assemblies for a Japanese firefly Aquatica lateralis and a bioluminescent click beetle, Ignelater luminosus. Analyses of these genomic datasets supports at least two independent gains of luminescence in beetles, and provides new insights into the evolution of beetle bioluminescence and chemical defenses that likely co-evolved over their 100 million years of evolution.

genomics↗

Discovery and reduction of nonspecific activities of the major herbicide-resistance gene BAR

Herbicide resistance is a major trait of genetically modified (GM) crops. Currently, resistance to phosphinothricin (also known as glufosinate) is the second most widespread genetically engineered herbicide-resistance trait in crops after glyphosate resistance1,2. Resistance to phosphinothricin in plants is achieved by transgenic expression of the bialaphos resistance (BAR) or phosphinothricin acetyltransferase (PAT) genes, which were initially isolated from the natural herbicide bialaphos-producing soil bacteria Streptomyces hygroscopicus and S. viridochromogenes, respectively3,4. Mechanistically, BAR and PAT encode phosphinothricin acetyltransferase, which transfers an acetyl group from acetyl coenzyme A (acetyl-CoA) to the -NH2 group of phosphinothricin, resulting in herbicide inactivation1. Although early in vitro enzyme assays showed that recombinant BAR and PAT exhibit substrate preference toward phosphinothricin over the 20 proteinogenic amino acids1, whether transgenic expression of BAR and PAT affects plant endogenous metabolism in vivo was not known. Combining metabolomics, plant genetics, and biochemical approaches, we show that transgenic BAR indeed converts two plant endogenous amino acids, aminoadipate and tryptophan, to their respective N-acetylated products in several plant species examined. We report the crystal structures of BAR, and further delineate structural basis for its substrate selectivity and catalytic mechanism. Through structure-guided protein engineering, we generated several BAR variants that display significantly reduced nonspecific activities compared to its wild-type counterpart. Our results demonstrate that transgenic expression of enzymes as a common strategy in modern biotechnology may render unintended metabolic consequences arisen from enzyme promiscuity. Understanding of such phenomena at the mechanistic level will facilitate better design of maximally insulated systems featuring heterologously expressed enzymes.

plant biology↗