TY - JOUR
T1 - Phylogenomic Mining of the Mints Reveals Multiple Mechanisms Contributing to the Evolution of Chemical Diversity in Lamiaceae
AU - Mint Evolutionary Genomics Consortium
AU - Boachon, Benoît
AU - Buell, C. Robin
AU - Crisovan, Emily
AU - Dudareva, Natalia
AU - Garcia, Nicolas
AU - Godden, Grant
AU - Henry, Laura
AU - Kamileen, Mohamed O.
AU - Kates, Heather Rose
AU - Lichman, Benjamin R.
AU - Kilgore, Matthew B.
AU - Mavrodiev, Evgeny V.
AU - Newton, Linsey
AU - Rodriguez-Lopez, Carlos
AU - O'Connor, Sarah E.
AU - Soltis, Douglas
AU - Soltis, Pamela
AU - Vaillancourt, Brieanne
AU - Wiegert-Rininger, Krystle
AU - Zhao, Dongyan
N1 - © The Author 2018
PY - 2018/8/6
Y1 - 2018/8/6
N2 - 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.
AB - 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.
KW - chemodiversity
KW - evolution
KW - iridoid
KW - terpene
UR - http://www.scopus.com/inward/record.url?scp=85050304473&partnerID=8YFLogxK
U2 - 10.1016/j.molp.2018.06.002
DO - 10.1016/j.molp.2018.06.002
M3 - Article
AN - SCOPUS:85050304473
SN - 1674-2052
VL - 11
SP - 1084
EP - 1096
JO - Molecular plant
JF - Molecular plant
IS - 8
ER -
