Unprecedented Utilization of Pelargonidin and Indole for the Biosynthesis of Plant Indole Alkaloids

Abstract

Nudicaulins are a group of indole alkaloid glycosides responsible for the color of yellow petals of Papaver nudicaule (Iceland poppy). The unique aglycone scaffold of these alkaloids attracted our interest as one of the most unusual flavonoid‐indole hybrid structures that occur in nature. Stable isotope labeling experiments with sliced petals identified free indole, but not tryptamine or l‐tryptophan, as one of the two key biosynthetic precursors of the nudicaulin aglycone. Pelargonidin was identified as the second key precursor, contributing the polyphenolic unit to the nudicaulin molecule. This finding was inferred from the temporary accumulation of pelargonidin glycosides in the petals during flower bud development and a drop at the point in time when nudicaulin levels start to increase. The precursor‐directed incorporation of cyanidin into a new 3′‐hydroxynudicaulin strongly supports the hypothesis that anthocyanins are involved in the biosynthesis of nudicaulins.

Biosynthetic and Functional Color–Scent Associations in Flowers of Papaver nudicaule and Their Impact on Pollinators

“…Although indole is consumed in the biosynthesis of nudicaulins, its level increased, though not to a statistically significant degree, during the development of yellow petals ( p =0.067). A previous study revealed that the maximum level of indole in yellow petals is reached shortly before flowering . These results suggest that, in yellow flowers, more indole is produced than is used for the synthesis of nudicaulins, and so it is emitted as a floral volatile.…”

“…Although their biosynthesis is not well studied, some reports suggest that they are products of the phenylpropanoid biosynthetic pathway . In P. nudicaule , this route is active during the production of pelargonidin, thus suggesting a second biochemical connection between floral volatiles and pigments in the flowers of this species.…”

“…Considering that indole is one of the final precursors of the nudicaulins, which are produced in the petals of the yellow cultivar, we asked if the petals were responsible for the emission of indole. Therefore, we collected the volatile compounds of petals and, separately, of capsules (including stamens, stigmatic disc, and ovaries) of yellow flowers.…”

“…Nudicaulins are a unique group of alkaloids characterized by a pentacyclic skeleton composed of an indole and a polyphenolic moiety . Indole and the pelargonidin glycosides are the final biosynthetic precursors of nudicaulins . All of these metabolites originate from shikimate, which is the precursor of both the indole and phenylpropanoid/plant polyketide pathways.…”

“…All of these metabolites originate from shikimate, which is the precursor of both the indole and phenylpropanoid/plant polyketide pathways. Drawing on current knowledge of flower pigments of P. nudicaule and nudicaulin biosynthesis in yellow petals, we studied the floral scent composition of four different cultivars and evaluated the impact of conserved biochemistry in the evolution of color–scent associations. Specifically, we investigated 1) whether there are specific volatile compounds associated with the flower pigments of four different P. nudicaule cultivars; and 2) how visual and olfactory cues provided by flowers of P. nudicaule affect how they are discriminated by a pollinator, such as the honeybee, Apis mellifera .…”