Genomic Insights into the Evolution of the Nicotine Biosynthesis Pathway in Tobacco

Abstract

In tobacco (Nicotiana tabacum), nicotine is the predominant alkaloid. It is produced in the roots and accumulated mainly in the leaves. Jasmonates play a central signaling role in damage-induced nicotine formation. The genome sequence of tobacco provides us an almost complete inventory of structural and regulatory genes involved in nicotine pathway. Phylogenetic and expression analyses revealed a series of structural genes of the nicotine pathway, forming a regulon, under the control of jasmonate-responsive ETHYLENE RESPONSE FACTOR (ERF) transcription factors. The duplication of NAD and polyamine metabolic pathways and the subsequent recruitment of duplicated primary metabolic genes into the nicotine biosynthesis regulon were suggested to be the drivers for pyridine and pyrrolidine ring formation steps early in the pathway. Transcriptional regulation by ERF and cooperatively acting MYC2 transcription factors are corroborated by the frequent occurrence of cognate cis-regulatory elements of the factors in the promoter regions of the downstream structural genes. The allotetraploid tobacco has homologous clusters of ERF genes on different chromosomes, which are possibly derived from two ancestral diploids and include either nicotine-controlling ERF189 or ERF199. A large chromosomal deletion was found within one allele of the nicotine-controlling NICOTINE2 locus, which is part of one of the ERF gene clusters, and which has been used to breed tobacco cultivars with a low-nicotine content.

HILIC HPLC‐ESI‐MS/MS identification and quantification of the alkaloids from the genus Equisetum

“…deterrence effect of herbivores seems rather unlikely. Therefore, it seems more likely that these low levels of nicotine are an unintended side product towards the biosynthesis of the primary metabolite NAD . These rather low concentrations, without any hint of biological activity are also known for other (food plants) like tea ( Camellia sinensis ), carrot, pear, strawberry or plants from the Solanaceae family (besides the well‐known Nicotiana spp.…”

“…Therefore, it seems more likely that these low levels of nicotine are an unintended side product towards the biosynthesis of the primary metabolite NAD. 34…”

Natural variations in the MYB transcription factor MYB31 determine the evolution of extremely pungent peppers

“…Plants have evolved numerous specialized metabolites that play essential roles in mediating interactions between plants and their habitats (Song et al ., ), and these compounds constitute a valuable resource for the discovery of economically important bioactive structures (Mithöfer & Boland, ; Shang et al ., ; Kajikawa et al ., ). Intriguingly, some plants have evolved fruit‐specific defensive chemicals to deter herbivores and prevent their fruits and seeds from being attacked by microbes (Tewksbury et al ., , ).…”

Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis

“…For instance, putrescine, an essential metabolite for all living organisms, serves as the branch point for the biosynthesis of different specialized metabolites in plants. The N-methylation of putrescine catalyzed by putrescine N-methyltransferase (PMT) is the branch point of the biosynthesis of ornithine-derived alkaloids such as nicotine, tropane and nortropane alkaloids (Junker et al, 2013;Kajikawa et al, 2017). The dimerization of putrescine by homospermidine synthase (HSS) on the other hand triggers the biosynthesis of pyrrolizidine alkaloids, which are distributed in a wide range of plant species (Ober and Hartmann, 1999;Ober et al, 2003).…”