Specific recognition, detoxification and metabolism of pyrrolizidine alkaloids by the polyphagous arctiid Estigmene acrea

• Published in: Insect biochemistry and molecular biology 2005-05, Vol.35 (5), p.391-411
• Main Authors: Hartmann, T., Theuring, C., Beuerle, T., Klewer, N., Schulz, S., Singer, M.S., Bernays, E.A.
• Format: Article
• Language: English
• Subjects: adaptation; alkaloid metabolism; Alkaloid processing; Alkaloid sequestration; Animals; Apocynaceae; Arctiidae; Asteraceae; Boraginaceae; chemical constituents of plants; Chemical defense; courtship; Crotalaria; Crotalaria - chemistry; defense mechanisms; Diet; Estigmene; Estigmene acrea; Estigmene acrea (Lepidoptera; Fabaceae; Feeding Behavior - physiology; Hydroxydanaidal; insect pheromones; Larva - metabolism; male courtship pheromone; metabolic detoxification; metabolic sequestration; Moths - metabolism; Orchidaceae; oxidation; Oxidation-Reduction; Pheromone; Pyrrolizidine alkaloids; Pyrrolizidine Alkaloids - chemistry; Pyrrolizidine Alkaloids - metabolism; retronecine; sensory receptors; sex pheromones; Taste receptor; taste receptors
• ISSN: 0965-1748; 1879-0240
• DOI: 10.1016/j.ibmb.2004.12.010

Evidence is presented that the polyphagous arctiid Estigmene acrea is well adapted to sequester and specifically handle pyrrolizidine alkaloids of almost all known structural types representative of the major plant families with pyrrolizidine alkaloid-containing species, i.e. Asteraceae with the tribes Senecioneae and Eupatorieae, Boraginaceae, Fabaceae, Apocynaceae and Orchidaceae. The adaptation of E. acrea to pyrrolizidine alkaloids includes a number of specialized characters: (i) highly sensitive recognition of alkaloid sources by pyrrolizidine alkaloid-specific taste receptors; (ii) detoxification of pyrrolizidine alkaloids by N -oxidation catalyzed by a specific flavin-dependent monooxygenase; (iii) transfer and maintenance of all types of pyrrolizidine N-oxides through all developmental stages; (iv) conversion of the various structures into the male courtship pheromone hydroxydanaidal most probably through retronecine and insect specific retronecine esters (creatonotines) as common intermediates; (v) specific integration into mating behavior and defense strategies. Toxic otonecine derivatives, e.g. the senecionine analogue senkirkine, which often accompany the common retronecine derivatives and which cannot be detoxified by N -oxidation do not affect the development of E. acrea larvae. Senkirkine is not sequestered at all. Non-toxic 1,2-saturated platynecine derivatives that frequently occur together with toxic retronecine esters are sequestered and metabolized to hydroxydanaidal, indicating the ability of E. acrea to aromatize saturated pyrrolizidines. Although pyrrolizidine alkaloids, even if they are offered continuously at a high level (2%) in the larval diet, are non-toxic, E. acrea larvae are not able to develop exclusively on a pyrrolizidine alkaloid-containing plant like Crotalaria. Therefore, E. acrea appears to be specifically adapted to exploit pyrrolizidine alkaloid-containing plants as “drug source” but not as a food source.