All plants synthesize a suite of several hundred terpenoid compounds with roles that include phytohormones, protein modification reagents, anti-oxidants, and more. Different plant lineages also ...synthesize hundreds of distinct terpenoids, with the total number of such specialized plant terpenoids estimated in the scores of thousands. Phylogenetically restricted terpenoids are implicated in defense or in the attraction of beneficial organisms. A popular hypothesis is that the ability of plants to synthesize new compounds arose incrementally by selection when, as a result of gradual changes in their biotic partners and enemies, the ‘old’ plant compounds were no longer effective, a process dubbed the ‘coevolutionary arms race’. Another hypothesis posits that often the sheer diversity of such compounds provides benefits that a single compound cannot. In this article, we review the unique features of the biosynthetic apparatus of terpenes in plants that facilitate the production of large numbers of distinct terpenoids in each species and how facile genetic and biochemical changes can lead to the further diversification of terpenoids. We then discuss evidence relating to the hypotheses that given ecological functions may be enhanced by the presence of mixtures of terpenes and that the acquisition of new functions by terpenoids may favor their retention once the original functions are lost.
Plants synthesize a multitude of compounds that contribute to adaptation to their ecological niches. Such compounds serve as attractants of other living organisms beneficial to the plants or as ...defense against other biotic as well as abiotic agents. Selection for increased fitness, a never-ending process, has resulted in each plant lineage synthesizing a distinct set of specialized metabolites appropriate for its environment. The total number of specialized metabolites found in the plant kingdom far exceeds the capacity of any one plant genome to encode the necessary enzymes, and just as a plant lineage acquires the ability to make new specialized compounds during evolution, it also loses the ability to make others. Although the ability of plants to make novel, specialized metabolites continues to evolve, there are also many examples in which different plants have independently evolved the ability to make compounds already present in other plant lineages or to make different compounds that fulfill the same role-both are examples of convergent evolution. Here, we discuss many examples of convergent evolution in specialized metabolism. There are many genetic and biochemical mechanisms that can give rise to convergent evolution, and we conclude that, overall, convergent evolution in plant specialized metabolism is surprisingly common.
Some plant terpenes such as sterols and carotenes are part of primary metabolism and found essentially in all plants. However, the majority of the terpenes found in plants are classified as ...‘secondary' compounds, those chemicals whose synthesis has evolved in plants as a result of selection for increased fitness via better adaptation to the local ecological niche of each species. Thousands of such terpenes have been found in the plant kingdom, but each species is capable of synthesizing only a small fraction of this total. In plants, a family of terpene synthases (TPSs) is responsible for the synthesis of the various terpene molecules from two isomeric 5-carbon precursor ‘building blocks', leading to 5-carbon isoprene, 10-carbon monoterpenes, 15-carbon sesquiterpenes and 20-carbon diterpenes. The bryophyte Physcomitrella patens has a single TPS gene, copalyl synthase/kaurene synthase (CPS/KS), encoding a bifunctional enzyme producing ent-kaurene, which is a precursor of gibberellins. The genome of the lycophyte Selaginella moellendorffii contains 18 TPS genes, and the genomes of some model angiosperms and gymnosperms contain 40-152 TPS genes, not all of them functional and most of the functional ones having lost activity in either the CPS- or KS-type domains. TPS genes are generally divided into seven clades, with some plant lineages having a majority of their TPS genes in one or two clades, indicating lineage-specific expansion of specific types of genes. Evolutionary plasticity is evident in the TPS family, with closely related enzymes differing in their product profiles, subcellular localization, or the in planta substrates they use.
Natural pyrethrin insecticides produced by Dalmatian pyrethrum (Tanacetum cinerariifolium) have low mammalian toxicity and short environmental persistence, providing an alternative to widely used ...synthetic agricultural insecticides that pose a threat to human health and the environment. A recent surge of interest in the use of pyrethrins as agricultural insecticides coincides with the discovery of several new genes in the pyrethrin biosynthetic pathway. Elucidation of this pathway facilitates efforts to breed improved pyrethrum varieties and to engineer plants with improved endogenous defenses or hosts for heterologous pyrethrin production. We describe the current state of knowledge related to global pyrethrum production, the pyrethrin biosynthetic pathway and its regulation, and recent efforts to engineer the pyrethrin pathway in diverse plant hosts.
Pyrethrin insecticides produced by Tanacetum cinerariifolium provide a human-safe and ecologically sound alternative to widely used synthetic insecticides.The development of transcriptomic and genomic resources for T. cinerariifolium facilitated the elucidation of numerous steps in the pyrethrin biosynthetic pathway.Pyrethrin biosynthetic genes have been engineered into diverse plant hosts; these efforts demonstrate the promise of engineering plants with improved endogenous defenses or of the development of an alternative source to pyrethrins for use as insecticides.
Plant volatiles (PVs) are lipophilic molecules with high vapor pressure that serve various ecological roles. The synthesis of PVs involves the removal of hydrophilic moieties and ...oxidation/hydroxylation, reduction, methylation, and acylation reactions. Some PV biosynthetic enzymes produce multiple products from a single substrate or act on multiple substrates. Genes for PV biosynthesis evolve by duplication of genes that direct other aspects of plant metabolism; these duplicated genes then diverge from each other over time. Changes in the preferred substrate or resultant product of PV enzymes may occur through minimal changes of critical residues. Convergent evolution is often responsible for the ability of distally related species to synthesize the same volatile.
Plants synthesize and emit a large variety of volatile organic compounds with terpenoids and fatty-acid derivatives the dominant classes. Whereas some volatiles are probably common to almost all ...plants, others are specific to only one or a few related taxa. The rapid progress in elucidating the biosynthetic pathways, enzymes, and genes involved in the formation of plant volatiles allows their physiology and function to be rigorously investigated at the molecular and biochemical levels. Floral volatiles serve as attractants for species-specific pollinators, whereas the volatiles emitted from vegetative parts, especially those released after herbivory, appear to protect plants by deterring herbivores and by attracting the enemies of herbivores.
Plants synthesize and emit many specialized volatile compounds to attract pollinators and to defend themselves against herbivores; the specific roles of these compounds and the pathways of their synthesis are now being elucidated.
All plants synthesize a diverse array of terpenoid metabolites. Some are common to all, but many are synthesized only in specific taxa and presumably evolved as adaptations to specific ecological ...conditions. While the basic terpenoid biosynthetic pathways are common in all plants, recent discoveries have revealed many variations in the way plants synthesized specific terpenes. A major theme is the much greater number of substrates that can be used by enzymes belonging to the terpene synthase (TPS) family. Other recent discoveries include non-TPS enzymes that catalyze the formation of terpenes, and novel transport mechanisms.
Plant trichomes come in a variety of shapes, sizes and cellular composition. Some types, commonly called glandular trichomes, produce large amounts of specialized (secondary) metabolites of diverse ...classes. Trichomes are implicated in a variety of adaptive processes, including defense against herbivores and micro-organisms as well as in ion homeostasis. Because trichomes protrude from the epidermis and can often be easily separated from it and harvested, the mRNAs, proteins and small molecules that they contain are unusually accessible to analysis. This property makes them excellent experimental systems for identification of the enzymes and pathways responsible for the synthesis of the specialized metabolites found in these structures and sometimes elsewhere in the plant. We review the literature on the biochemistry of trichomes and consider the attributes that might make them highly useful targets for plant metabolic engineering.
SUMMARY
Floral scent plays a crucial role in the reproductive process of many plants. Humans have been fascinated by floral scents throughout history, and have transported and traded floral scent ...products for which they have found multiple uses, such as in food additives, hygiene and perfume products, and medicines. Yet the scientific study of how plants synthesize floral scent compounds began later than studies on most other major plant metabolites, and the first report of the characterization of an enzyme responsible for the synthesis of a floral scent compound, namely linalool in Clarkia breweri, a California annual, appeared in 1994. In the almost 30 years since, enzymes and genes involved in the synthesis of hundreds of scent compounds from multiple plant species have been described. This review recapitulates this history and describes the major findings relating to the various aspects of floral scent biosynthesis and emission, including genes and enzymes and their evolution, storage and emission of scent volatiles, and the regulation of the biochemical processes.
Significance Statement
This reviews describes our existing knowledge of how flowers produce and emit volatile compounds, and discusses the reasons for why research in this area lagged behind other topics in plant biochemistry.
• Analysis of the updated reference tomato genome found 34 full-length TPS genes and 18 TPS pseudogenes.
• Biochemical analysis has now identified the catalytic activities of all enzymes encoded by ...the 34 TPS genes: one isoprene synthase, 10 exclusively or predominantly monoterpene synthases, 17 sesquiterpene synthases and six diterpene synthases. Among the monoterpene and sesquiterpene and diterpene synthases, some use trans-prenyl diphosphates, some use cis-prenyl diphosphates and some use both. The isoprene synthase is cytosolic; six monoterpene synthases are plastidic, and four are cytosolic; the sesquiterpene synthases are almost all cytosolic, with the exception of one found in the mitochondria; and three diterpene synthases are found in the plastids, one in the cytosol and two in the mitochondria.
• New trans-prenyltransferases (TPTs) were characterised; together with previously characterised TPTs and cis-prenyltransferases (CPTs), tomato plants can make all cis and trans C10, C15 and C20 prenyl diphosphates. Every type of plant tissue examined expresses some TPS genes and some TPTs and CPTs.
• Phylogenetic comparison of the TPS genes from tomato and Arabidopsis shows expansions in each clade of the TPS gene family in each lineage (and inferred losses), accompanied by changes in subcellular localisations and substrate specificities.
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