Metabolism, excretion and avoidance of cyanogenic glucosides in insects with different feeding specialisations.
Cyanogenic glucosides (CNglcs) are widespread plant defence compounds releasing toxic hydrogen cyanide when hydrolysed by specific β-glucosidases after plant tissue damage. In contrast to specialist herbivores that have mechanisms to avoid toxicity from CNglcs, it is generally assumed that non-adapted herbivores are negatively affected by CNglcs. Recent evidence, however, implies that the defence potential of CNglcs towards herbivores may not be as effective as previously anticipated. Here, performance, metabolism and excretion products of insects not adapted to CNglcs were analysed, including species with different degrees of dietary specialisation (generalists, specialists) and different feeding modes (leaf-snipping lepidopterans, piercing-sucking aphids). Insects were reared either on cyanogenic or acyanogenic plants or on an artificial cyanogenic diet. Lepidopteran generalists (Spodoptera littoralis, Spodoptera exigua, Mamestra brassicae) were compared to lepidopteran glucosinolate-specialists (Pieris rapae, Pieris brassicae, Plutella xylostella), and a generalist aphid (Myzus persicae) was compared to an aphid glucosinolate-specialist (Lipaphis erysimi). All insects were tolerant to cyanogenic plants; in lepidopterans tolerance was mainly due to excretion of intact CNglcs. The two Pieris species furthermore metabolized aromatic CNglcs to amino acid conjugates (Cys, Gly, Ser) and derivatives of these, which is similar to the metabolism of benzylglucosinolates in these species. Aphid species avoided uptake of CNglcs during feeding. Our results imply that non-adapted insects tolerate plant CNglcs either by keeping them intact for excretion, metabolizing them, or avoiding uptake.
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark. Electronic address: spentzold@ice.mpg.de.
Stefan
S
Pentzold
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark. Electronic address: miz@plen.ku.dk.
Mika
M
Zagrobelny
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark. Electronic address: nnb@plen.ku.dk.
Nanna
N
Bjarnholt
Ecologie Systématique Evolution, CNRS/Université Paris-Sud/AgroParisTech, Université Paris-Saclay, 91400, Orsay, France. Electronic address: juergen.kroymann@u-psud.fr.
Juergen
J
Kroymann
Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany. Electronic address: hvogel@ice.mpg.de.
Heiko
H
Vogel
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark. Electronic address: ceo@plen.ku.dk.
Carl Erik
CE
Olsen
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; Carlsberg Laboratory, Gamle Carlsberg Vej 10, DK-1799, Copenhagen V, Denmark. Electronic address: blm@plen.ku.dk.
Birger Lindberg
BL
Møller
Plant Biochemistry Laboratory, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Copenhagen, Denmark; VILLUM Research Center "Plant Plasticity", University of Copenhagen, Frederiksberg C, Copenhagen, Denmark. Electronic address: bak@plen.ku.dk.
Søren
S
Bak
D000222:Adaptation, Physiological; D000818:Animals; D005243:Feces / Q000737:chemistry; D005247:Feeding Behavior; D005960:Glucosides / Q000378:metabolism*; D060434:Herbivory / Q000502:physiology*; D006856:Hydrogen Cyanide / Q000378:metabolism*; D007313:Insecta / Q000378:metabolism*; D007814:Larva / Q000378:metabolism; D010944:Plants / Q000378:metabolism*
D005960:Glucosides; D006856:Hydrogen Cyanide
Cyanogenic glucosides; Generalists; Herbivory; Metabolism; Specialists; β-Glucosidases