Progress in disentangling the diversity of iridoids within the genus Nepeta: surprising biosynthetic and evolutionary insights

Abstract

Nepeta L. is the largest genus of the Lamiaceae family, and the exclusive representative of the subfamily Nepetoidae which produces iridoids. However, the genus Nepeta comprises both taxa producing iridoids (iridoid aglycones-IAs and/or iridoid glucosides-IGs), and those lacking iridoids. Combining omics-guided approach and functional genomics in elucidating the genetic background of the iridoid diversity within the genus Nepeta, we provide novel insights into molecular mechanisms driving the iridoid biosynthesis, and thus into chemical evolution of iridoids within the genus Nepeta. Multidisciplinary experimental approach is here explained on the example of iridoid synthases (IS), functionally characterized by in vitro enzymatic assays using recombinant proteins heterologously expressed in Escherichia coli. Functional ISs are expressed in both iridoid-producing N. rtanjensis (NrIS2) and N. sibirica L. (NsIS), as well as in iridoid-lacking N. nervosa L. (NnIS). N. nervosa possesses an iridoid biosynthetic platform, but inactive one, most likely due to the “switching off” or “silencing” of some gene(s) upstream in the pathway, which suggests that this species has lost the ability to produce iridoids during the evolution. Furthermore, comparative iridoid profiling and co-expression analysis of biosynthetic genes and transcription factors (TFs) during the exposure of chemodiverse Nepeta taxa to environmental stresses (e.g. dehydration, UV−B radiation, pathogens) or elicitors (MeJA), facilitated the explanation of regulatory mechanisms determining the productivity of plants, as well as of factors responsible for the presence/ absence of iridoids or specific groups of iridoids (IAs and IGs), in these plants.