The Scaffold-Forming Steps of Plant Alkaloid Biosynthesis

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The Scaffold-Forming Steps of Plant Alkaloid Biosynthesis Natural Product Reports View Article Online REVIEW View Journal | View Issue The scaffold-forming steps of plant alkaloid biosynthesis Cite this: Nat. Prod. Rep.,2021,38,103 Benjamin R. Lichman * Alkaloids from plants are characterised by structural diversity and bioactivity, and maintain a privileged position in both modern and traditional medicines. In recent years, there have been significant advances in elucidating the biosynthetic origins of plant alkaloids. In this review, I will describe the progress made in determining the metabolic origins of the so-called true alkaloids, specialised metabolites derived from Received 31st May 2020 amino acids containing a nitrogen heterocycle. By identifying key biosynthetic steps that feature in the DOI: 10.1039/d0np00031k majority of pathways, I highlight the key roles played by modifications to primary metabolism, iminium rsc.li/npr reactivity and spontaneous reactions in the molecular and evolutionary origins of these pathways. Creative Commons Attribution 3.0 Unported Licence. 1. Introduction 5. Mannich-like reaction 1.1. Background 5.1. Polyamine-derived 1.2. Denition of alkaloids 5.1.1. Polyketide 1.3. Major alkaloid classes 5.1.2. Nicotiana 1.4. Patterns in biosynthesis 5.1.3. Dimerisation 2. Amine accumulation 5.1.4. Pyrrolizidine formation 2.1. Polyamines 5.2. Aromatic amino-acid derived 2.1.1. Putrescine 5.2.1. Tetrahydroisoquinolines b This article is licensed under a 2.1.2. Cadaverine 5.2.2. -Carbolines 2.1.3. Homospermidine 5.2.3. Reduction 2.2. Aromatic amines 6. Discussion 2.2.1. Tyrosine 6.1. Precursor accumulation Open Access Article. Published on 03 August 2020. Downloaded 9/24/2021 8:32:53 AM. 2.2.2. Tryptophan 6.2. Subcellular localisation 2.3. Summary 6.3. Spontaneous reactions 3. Aldehyde accumulation 6.4. Enzyme evolution 3.1. Amino aldehydes 6.5. Pathway evolution 3.1.1. N-Methylaminobutanal and N-methylpyrrolinium 7. Conclusion 3.1.2. 5-Aminopentanal and D1-piperideine 8. Conicts of interest 3.1.3. 4-(4-Oxobutylamino)butanal and pyrrolizidine 9. Acknowledgements 3.2. Amino acid origins 10. References 3.2.1. Phenylacetaldehydes 3.2.2. Betalamic acid 3.3. Phenylpropanoids 3.3.1. Benzaldehydes 1. Introduction 3.3.2. Dihydrocinnamaldehyes 1.1. Background 3.4. Secologanin Alkaloids from plants have remarkable powers to harm, heal 4. Iminium formation and reveal; this has led to their use in herbal medicine and 4.1. Intramolecular related practises across continents and cultures for millennia. 4.2. Intermolecular Alkaloids were foundational in the development of organic 4.2.1. Coupled reactions chemistry and were among the rst pharmaceuticals developed. 4.2.2. Stable iminium They retain a privileged position in modern medicine, used widely to treat pain, cancer, dementia and countless other 1,2 Centre for Novel Agricultural Products, Department of Biology, University of York, York ailments (Fig. 1). Despite losing pace to synthetic drug YO10 5DD, UK. E-mail: [email protected] discovery approaches in recent decades, plant alkaloids remain This journal is © The Royal Society of Chemistry 2021 Nat. Prod. Rep.,2021,38,103–129 | 103 View Article Online Natural Product Reports Review Fig. 2 Types of alkaloids. Sparteine and quinine are true alkaloids, Fig. 1 Examples of pharmaceutical alkaloids. derived from lysine and tryptophan respectively. Mescaline is a proto- alkaloid. Coniine and aconitine are pseudo-alkaloids, with the nitrogen inserted through transamination. a viable source of bioactive compounds with considerable therapeutic potential.3 Creative Commons Attribution 3.0 Unported Licence. It is only through the elucidation of plant alkaloid biosyn- nature compounds.9,10 Genes and pathways can be heterolo- thesis—determining chemical intermediates, characterising gously expressed in genetically tractable and rapidly growing enzymes and sequencing genomes—that we can truly appre- organisms in an attempt to increase alkaloid yield, purity or ciate and understand the synthetic ingenuity of nature in con- access new-to-nature compounds through pathway modica- – structing these complex compounds. There has been tions.11 13 Understanding the genomic basis for alkaloid remarkable progress in the discovery and characterisation of biosynthesis can also inform efforts to breed plants with higher enzymes over the last decade, triggered by advances and compound yields or lower toxicity.14 expanded use of sequencing technologies.4,5 Genome assem- This article is licensed under a blies of alkaloid producing plants have revealed certain 1.2. Denition of alkaloids biosynthetic genes co-localise in clusters, aiding gene discovery Alkaloids were originally dened as alkaline substances and providing insight into evolution and pathway regulation.6–8 extracted from a plant with a biological activity.15 This de- The investigation of plant alkaloid biosynthesis can lead to Open Access Article. Published on 03 August 2020. Downloaded 9/24/2021 8:32:53 AM. nition has been rened multiple times to include compounds new tools and technologies. For example, enzymes can be from outside the plant kingdom, as well as those that share employed as biocatalysts for the in vitro formation of new-to- a biosynthetic origin with alkaloids but do not have a basic nitrogen.16,17 In the broadest sense, alkaloids are nitrogen- containing compounds derived from secondary, or speci- Dr Benjamin Lichman received alised, metabolism. However, it is useful to categorise alka- his MSc in Natural Sciences from loids further, not with the intention of excluding the University of Cambridge and compounds, but to help comprehend similarities and his PhD in biochemistry from differences in the compounds' origins (Fig. 2). The true University College London. His alkaloids, referred to as complex alkaloids in this review, are doctoral research, under the compounds in which the nitrogen atom is derived from an guidance of Professors John Ward amino acid and is part of a heterocycle. Proto-alkaloids, or and Helen Hailes, focussed on simple alkaloids, are amines derived from amino acids but the mechanism and applications do not have a nitrogen heterocycle. Pseudo-alkaloids are of norcoclaurine synthase. He nitrogen-containing metabolites in which the nitrogen is then joined the group of Prof introduced at a late stage through an enzymatic process such Sarah O'Connor at the John Innes as transamination. Centre to investigate iridoid biosynthesis in plants. In 2018 he was appointed a lecturer at the Centre for Novel Agricultural Products at the University of York. 1.3. Major alkaloid classes Benjamin is currently a UKRI Future Leaders Fellow and manages This review focusses on complex ‘true’ alkaloids from plants: a research group investigating the origins and applications of plant compounds derived from an amino acid containing natural product biosynthesis. a nitrogen heterocycle. Despite their wide structural diversity 104 | Nat. Prod. Rep.,2021,38,103–129 This journal is © The Royal Society of Chemistry 2021 View Article Online Review Natural Product Reports Scheme 1 Themes in complex alkaloid biosynthesis explored in this review. and taxonomic distribution, the biosynthetic origins of these principles of biosynthesis discussed in this review can be compounds follows a unifying chemical logic centred around applied to many alkaloid families not directly mentioned. the formation and reactivity of the iminium cation.18 Iwill examine the rst steps of alkaloid biosynthetic pathways: the 1.4. Patterns in biosynthesis transition from primary to specialised metabolism and The rst steps in an alkaloid pathway are the most crucial, formation of the dening scaffold. The metabolic, enzymatic acting as the gateway to a new chemical space. They are Creative Commons Attribution 3.0 Unported Licence. and evolutionary origins of these steps will be reviewed, important metabolically, as they direct ux away from primary including the latest developments in the eld. and into specialised metabolism. They are signicant chemi- This review will cover all major complex alkaloid families in cally and enzymatically as they involve the formation of a new plants. Compounds derived from tyrosine include benzyliso- molecular structure. They also play a foundational role in the quinolines, tetrahydroisoquinolines and the Amaryllidaceae evolution of the pathways. alkaloids. Although not classically described as alkaloids, the There are four steps that are typically present in the rst steps tyrosine-derived betalains share many biosynthetic features of complex alkaloid biosynthesis: (i) accumulation of an amine with alkaloids and will be discussed. The tryptophan-derived precursor, (ii) accumulation of an aldehyde precursor, (iii) monoterpene indole alkaloids are included. The anthranilate This article is licensed under a formation of an iminium cation and (iv) a Mannich-like reaction derived acridone and quinoline alkaloids are only briey (Scheme 1). This nal step is oen considered the “scaffold- mentioned, as they do not subscribe to the biosynthetic forming”, signature, or rst-committed step into a pathway. patterns described in this review. Polyamine derived alkaloids A major origin of variation in these generalised steps is Open Access Article. Published on 03 August 2020. Downloaded 9/24/2021 8:32:53 AM. including piperideine, tropane, quinolizidine, pyrrolizidine and whether they are intermolecular or intramolecular (Table 1). For Nicotiana alkaloids are all included. It is hoped that the example, polyamine-derived alkaloids generally
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