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Abstract The spatial organization of genes within plant genomes can drive evolution of specialized metabolic pathways. Terpenoids are important specialized metabolites in plants with diverse adaptive functions that enable environmental interactions. Here, we report the genome assemblies of Prunella vulgaris , Plectranthus barbatus , and Leonotis leonurus . We investigate the origin and subsequent evolution of a diterpenoid biosynthetic gene cluster (BGC) together with other seven species within the Lamiaceae (mint) family. Based on core genes found in the BGCs of all species examined across the Lamiaceae, we predict a simplified version of this cluster evolved in an early Lamiaceae ancestor. The current composition of the extant BGCs highlights the dynamic nature of its evolution. We elucidate the terpene backbones generated by the Callicarpa americana BGC enzymes, including miltiradiene and the terpene (+)-kaurene, and show oxidization activities of BGC cytochrome P450s. Our work reveals the fluid nature of BGC assembly and the importance of genome structure in contributing to the origin of metabolites.more » « less
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Summary In plants, the biosynthetic pathways of some specialized metabolites are partitioned into specialized or rare cell types, as exemplified by the monoterpenoid indole alkaloid (MIA) pathway ofCatharanthus roseus(Madagascar Periwinkle), the source of the anticancer compounds vinblastine and vincristine. In the leaf, theC. roseusMIA biosynthetic pathway is partitioned into three cell types with the final known steps of the pathway expressed in the rare cell type termed idioblast. How cell‐type specificity of MIA biosynthesis is achieved is poorly understood.We generated single‐cell multi‐omics data fromC. roseusleaves. Integrating gene expression and chromatin accessibility profiles across single cells, as well as transcription factor (TF)‐binding site profiles, we constructed a cell‐type‐aware gene regulatory network for MIA biosynthesis.We showcased cell‐type‐specific TFs as well as cell‐type‐specificcis‐regulatory elements. Using motif enrichment analysis, co‐expression across cell types, and functional validation approaches, we discovered a novel idioblast‐specific TF (Idioblast MYB1,CrIDM1) that activates expression of late‐stage MIA biosynthetic genes in the idioblast.These analyses not only led to the discovery of the first documented cell‐type‐specific TF that regulates the expression of two idioblast‐specific biosynthetic genes within an idioblast metabolic regulon but also provides insights into cell‐type‐specific metabolic regulation.more » « less
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SUMMARY Single‐parent expression (SPE) is defined as gene expression in only one of the two parents. SPE can arise from differential expression between parental alleles, termed non‐presence/absence (non‐PAV) SPE, or from the physical absence of a gene in one parent, termed PAV SPE. We used transcriptome data of diverseZea mays(maize) inbreds and hybrids, including 401 samples from five different tissues, to test for differences between these types of SPE genes. Although commonly observed, SPE is highly genotype and tissue specific. A positive correlation was observed between the genetic distance of the two inbred parents and the number of SPE genes identified. Regulatory analysis showed that PAV SPE and non‐PAV SPE genes are mainly regulated byciseffects, with a small fraction undertransregulation. Polymorphic transposable element insertions in promoter sequences contributed to the high level ofcisregulation for PAV SPE and non‐PAV SPE genes. PAV SPE genes were more frequently expressed in hybrids than non‐PAV SPE genes. The expression of parentally silent alleles in hybrids of non‐PAV SPE genes was relatively rare but occurred in most hybrids. Non‐PAV SPE genes with expression of the silent allele in hybrids are more likely to exhibit above high parent expression level than hybrids that do not express the silent allele, leading to non‐additive expression. This study provides a comprehensive understanding of the nature of non‐PAV SPE and PAV SPE genes and their roles in gene expression complementation in maize hybrids.more » « less
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