Phylogenomic Mining of the Mints Reveals Multiple Mechanisms Contributing to the Evolution of Chemical Diversity in Lamiaceae

The evolution of chemical complexity has been a major driver of plant diversification, with novel compounds serving as key innovations. The species-rich mint family (Lamiaceae) produces an enormous variety of compounds that act as attractants and defense molecules in nature and are used widely by humans as flavor additives, fragrances, and anti-herbivory agents. To elucidate the mechanisms by which such diversity evolved, we combined leaf transcriptome data from 48 Lamiaceae species and four outgroups with a robust phylogeny and chemical analyses of three terpenoid classes (monoterpenes, sesquiterpenes, and iridoids) that share and compete for precursors. Our integrated chemical–genomic–phylogenetic approach revealed that: (1) gene family expansion rather than increased enzyme promiscuity of terpene synthases is correlated with mono- and sesquiterpene diversity; (2) differential expression of core genes within the iridoid biosynthetic pathway is associated with iridoid presence/absence; (3) generally, production of iridoids and canonical monoterpenes appears to be inversely correlated; and (4) iridoid biosynthesis is significantly associated with expression of geraniol synthase, which diverts metabolic flux away from canonical monoterpenes, suggesting that competition for common precursors can be a central control point in specialized metabolism. These results suggest that multiple mechanisms contributed to the evolution of chemodiversity in this economically important family. The mint family (Lamiaceae) includes many culturally and economically important species and collectively exhibits an exceptionally high degree of chemical diversity. Using an integrated chemical-genomic-phylogenetic approach, gene family expansion, altered gene expression of key biosynthetic pathway genes, and flux of precursors were shown to underlie the evolution of chemodiversity observed in this chemically rich clade

gel_v1.transcripts.fasta

Gelsemium sempervirens (version 1) transcript sequence

gel_v1.proteins.fasta

Gelsemium sempervirens (version 1) protein sequence

cro_v2.transcripts.fasta

Catharanthus roseus (version 2) transcript sequence

Data from: Gene discovery in Gelsemium highlights conserved gene clusters in monoterpene indole alkaloid biosynthesis

No description availabl

cro_v2_asm.fasta

Genome assembly of Catharanthus roseus (version 2), containing 2,090 scaffold sequence

cro_v2.gene_models.gff3

Gene Model Annotation for Catharanthus roseus (version 2) in Generic Feature Format 3 (GFF3

cro_v2.proteins.fasta

Catharanthus roseus (version 2) protein sequence

LC-MS data of 52 Lamiales species.zip

LC-MS data from all 52 species (Zipped folder)