The rise of operon-like gene clusters in plants

•Gene clusters in plants encode secondary metabolites implicated in defense. •Clustering of entire pathways facilitates co-inheritance and co-regulation. •Cluster prediction and regulation studies require a multidisciplinary approach. •Cluster knowledge can serve crop biofortification and industrial production. Gene clusters are common features of prokaryotic genomes also present in eukaryotes. Most clustered genes known are involved in the biosynthesis of secondary metabolites. Although horizontal gene transfer is a primary source of prokaryotic gene cluster (operon) formation and has been reported to occur in eukaryotes, the predominant source of cluster formation in eukaryotes appears to arise de novo or through gene duplication followed by neo- and sub-functionalization or translocation. Here we aim to provide an overview of the current knowledge and open questions related to plant gene cluster functioning, assembly, and regulation. We also present potential research approaches and point out the benefits of a better understanding of gene clusters in plants for both fundamental and applied plant science. Gene clusters are common features of prokaryotic genomes also present in eukaryotes. Most clustered genes known are involved in the biosynthesis of secondary metabolites. Although horizontal gene transfer is a primary source of prokaryotic gene cluster (operon) formation and has been reported to occur in eukaryotes, the predominant source of cluster formation in eukaryotes appears to arise de novo or through gene duplication followed by neo- and sub-functionalization or translocation. Here we aim to provide an overview of the current knowledge and open questions related to plant gene cluster functioning, assembly, and regulation. We also present potential research approaches and point out the benefits of a better understanding of gene clusters in plants for both fundamental and applied plant science. a set of two or more non-homologous genes encoding enzymes from the same pathway (to be distinguished from the gene clusters resulting from tandem duplication and consisting of homologous genes). Hox transcription factors control the body plan of an embryo along the anterior–posterior axis. Hox proteins are able to bind specific DNA sequences and can activate or repress a gene. The highly conserved homeodomain (60 amino acids), part of Hox, confers the ability to bind DNA. In vertebrates, the Hox genes are situated in groups or clusters and their expression can be characterized with spatial (the order of genes on the chromosome corresponds to the region of expression in the body) and temporal colinearity (activation of the separate genes starts at the 3′-end of the cluster and moves towards the 5′-end). transfer of genetic material between organisms that occurs in a way that is different from reproduction (vertical gene transfer); also known as lateral gene transfer. a set of proteins encoded by a large gene family in all vertebrates. The MHC mediates leukocyte interactions and is thus involved in immunity. It determines organ donor recipient compatibility and one's susceptibility to autoimmune disease, it is expressed codominantly (both sets of alleles are inherited) and can vary considerably between different organisms within a species (polymorphic). The MHC gene family has three subgroups: class I, class II, and class III. The genes are divided into clusters and superclusters. In humans, MHC is also known as human leukocyte antigen (HLA). a messenger RNA (mRNA) molecule is said to be monocistronic when it contains the information for the translation of a single protein (polypeptide): one open reading frame (ORF). A polycistronic mRNA contains multiple ORFs and is often regulated by a single promoter and translated into several polypeptides that can have related functions. a cluster of genes under the control of a single regulatory element. The genes are usually transcribed as one polycistronic mRNA, which can either be translated together or undergo trans-splicing resulting in several monocistronic mRNAs that are translated separately into proteins. Operons were originally thought to exist only in prokaryotes but are also found in eukaryotes (e.g., Caenorhabditis elegans). a large cluster of biosynthetic genes with related functions in close proximity to one another. a term used to describe the colocalization of several genetic loci on one chromosome in an organism or species; can also be employed to indicate conservation of gene order between two or more sets of chromosomes of different species. mobile genetic elements that can change their positions within the genome. TEs are divided into two classes, I and II, known as ‘copy and paste’ and ‘cut and paste’. Class I TEs (retrotransposons) are first transcribed from DNA to RNA and then reverse-transcribed to DNA. Class II TEs are DNA transposons; the mechanism of which does not involve an RNA intermediate. a form of RNA processing (splicing) found in eukaryotes during which exons from two different RNA primary transcripts are joined together; to be distinguished from cis-splicing where all the exons in the mature RNA molecule come from the same primary transcript.