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Interestingly, pairing of protein functionality in plant defense can also occur in the form of fusion of functional domains within a single protein; nucleotide-binding leucine-rich repeat (NLR) proteins, involved in pathogen recognition, can be fused with various protein domains that serve as baits for pathogen effectors [12]. The specialized metabolites encoded by these BGCs have diverse modes of action, for example, disrupting pathogen cell membranes [16], conferring bitterness or toxicity that deters herbivores [17,18], undergoing pathogen-induced degradation to give bioactive volatiles [19], or forming physical barriers against biotic and abiotic stress factors [20]. [...]benzoxazinoids (defense compounds produced by grasses and some eudicots) have been implicated in regulation of defense responses, flowering time, auxin metabolism, and iron uptake in maize [32]; cyanogenic glycosides serve as nitrogen storage compounds in the rubber tree [33]; and perturbation of the pathway for the oat defense compound avenacin A-1 can result in accumulation of the precursor β-amyrin with associated effects on root epidermal cell patterning [34]. Genomic factors that may contribute to the formation, regulation, and evolution of BGCs include transposable element-mediated recombination [37], chromosomal inversion [38], gene shuffling [39,40], whole genome duplications [41,42], copy number variations of genes within BGCs [43], chromatin modification [44,45], and chromosomal 3D structure [46].

Terpenoids are the most structurally diverse class of plant natural products with a huge range of commercial and medical applications. Exploiting this enormous potential has historically been hindered due to low levels of these compounds in their natural sources, making isolation difficult, while their structural complexity frequently makes synthetic chemistry approaches uneconomical. Engineering terpenoid biosynthesis in heterologous host production platforms provides a means to overcome these obstacles. In particular, plant-based production systems are attractive as they provide the compartmentalisation and cofactors necessary for the transfer of functional pathways from other plants. Nicotiana benthamiana , a wild relative of tobacco, has become increasingly popular as a heterologous expression platform for reconstituting plant natural product pathways, because it is amenable to Agrobacterium- mediated transient expression, a scalable and highly flexible process that enables rapid expression of genes and enzymes from other plant species. Here, we review recent work describing terpene production in N. benthamiana . We examine various strategies taken to engineer this host for increased production of the target metabolite. We also look at how transient expression can be utilised for rapid generation of molecular diversity, including new-to-nature products. Finally, we highlight current issues surrounding this expression platform and discuss the future directions and developments which will be needed to fully realise the potential of this system.

Operons are clusters of unrelated genes with related functions that are a feature of prokaryotic genomes. Here, we report on an operon-like gene cluster in the plant Arabidopsis thaliana that is required for triterpene synthesis (the thalianol pathway). The clustered genes are coexpressed, as in bacterial operons. However, despite the resemblance to a bacterial operon, this gene cluster has been assembled from plant genes by gene duplication, neofunctionalization, and genome reorganization, rather than by horizontal gene transfer from bacteria. Furthermore, recent assembly of operon-like gene clusters for triterpene synthesis has occurred independently in divergent plant lineages (Arabidopsis and oat). Thus, selection pressure may act during the formation of certain plant metabolic pathways to drive gene clustering.

Genomics-based predictions indicate that plants harbor the ability to make a vast array of as yet undiscovered chemistry. Recent advances open up the potential to harness this capability at unprecedented scale for the discovery and development of new therapeutics.

Operons (clusters of co-regulated genes with related functions) are common features of bacterial genomes. More recently, functional gene clustering has been reported in eukaryotes, from yeasts to filamentous fungi, plants, and animals. Gene clusters can consist of paralogous genes that have most likely arisen by gene duplication. However, there are now many examples of eukaryotic gene clusters that contain functionally related but non-homologous genes and that represent functional gene organizations with operon-like features (physical clustering and co-regulation). These include gene clusters for use of different carbon and nitrogen sources in yeasts, for production of antibiotics, toxins, and virulence determinants in filamentous fungi, for production of defense compounds in plants, and for innate and adaptive immunity in animals (the major histocompatibility locus). The aim of this article is to review features of functional gene clusters in prokaryotes and eukaryotes and the significance of clustering for effective function.

Plant natural products are of great value for agriculture, medicine and a wide range of other industrial applications. The discovery of new plant natural product pathways is currently being revolutionized by two key developments. First, breakthroughs in sequencing technology and reduced cost of sequencing are accelerating the ability to find enzymes and pathways for the biosynthesis of new natural products by identifying the underlying genes. Second, there are now multiple examples in which the genes encoding certain natural product pathways have been found to be grouped together in biosynthetic gene clusters within plant genomes. These advances are now making it possible to develop strategies for systematically mining multiple plant genomes for the discovery of new enzymes, pathways and chemistries. Increased knowledge of the features of plant metabolic gene clusters – architecture, regulation and assembly – will be instrumental in expediting natural product discovery. This review summarizes progress in this area.

The chemical diversity within the plant kingdom is likely to be a consequence of niche colonization and adaptive evolution. Plant-derived natural products have important functions in defense. They also have broader ecological roles and may in addition participate in plant growth and development. Recent data suggest that some antimicrobial phytochemicals may not serve simply as chemical barriers but could also have functions in defense-related signaling processes. It is important, therefore, that we should not to be too reductionist in our thinking when endeavoring to understand the forces and mechanisms that drive chemical diversification in plants.

In bacteria, genes with related functions often are grouped together in operons and are cotranscribed as a single polycistronic mRNA. In eukaryotes, functionally related genes generally are scattered across the genome. Notable exceptions include gene clusters for catabolic pathways in yeast, synthesis of secondary metabolites in filamentous fungi, and the major histocompatibility complex in animals. Until quite recently it was thought that gene clusters in plants were restricted to tandem duplicates (for example, arrays of leucine-rich repeat disease-resistance genes). However, operon-like clusters of coregulated nonhomologous genes are an emerging theme in plant biology, where they may be involved in the synthesis of certain defense compounds. These clusters are unlikely to have arisen by horizontal gene transfer, and the mechanisms behind their formation are poorly understood. Previously in thale cress (Arabidopsis thaliana) we identified an operon-like gene cluster that is required for the synthesis and modification of the triterpene thalianol. Here we characterize a second operon-like triterpene cluster (the marneral cluster) from A. thaliana, compare the features of these two clusters, and investigate the evolutionary events that have led to cluster formation. We conclude that common mechanisms are likely to underlie the assembly and control of operon-like gene clusters in plants.

Numerous examples of biosynthetic gene clusters (BGCs), including for compounds of agricultural and medicinal importance, have now been discovered in plant genomes. However, little is known about how these complex traits are assembled and diversified. Here, we examine a large number of variants within and between species for a paradigm BGC (the thalianol cluster), which has evolved recently in a common ancestor of the Arabidopsis genus. Comparisons at the species level reveal differences in BGC organization and involvement of auxiliary genes, resulting in production of species-specific triterpenes. Within species, the thalianol cluster is primarily fixed, showing a low frequency of deleterious haplotypes. We further identify chromosomal inversion as a molecular mechanism that may shuffle more distant genes into the cluster, so enabling cluster compaction. Antagonistic natural selection pressures are likely involved in shaping the occurrence and maintenance of this BGC. Our work sheds light on the birth, life and death of complex genetic and metabolic traits in plants. How plant biosynthetic gene clusters (BGCs) form and evolve remains unclear. Here, via examining available genomes within and between Arabidopsis species, the authors show that the thalianol BGC has evolved recently and is still dynamically evolving through involvement of auxiliary genes and chromosomal inversions.