Gene duplications circumvent trade-offs in enzyme function: Insect adaptation to toxic host plants.
Herbivorous insects and their adaptations against plant toxins provide striking opportunities to investigate the genetic basis of traits involved in coevolutionary interactions. Target site insensitivity to cardenolides has evolved convergently across six orders of insects, involving identical substitutions in the Na,K-ATPase gene and repeated convergent gene duplications. The large milkweed bug, Oncopeltus fasciatus, has three copies of the Na,K-ATPase α-subunit gene that bear differing numbers of amino acid substitutions in the binding pocket for cardenolides. To analyze the effect of these substitutions on cardenolide resistance and to infer possible trade-offs in gene function, we expressed the cardenolide-sensitive Na,K-ATPase of Drosophila melanogaster in vitro and introduced four distinct combinations of substitutions observed in the three gene copies of O. fasciatus. With an increasing number of substitutions, the sensitivity of the Na,K-ATPase to a standard cardenolide decreased in a stepwise manner. At the same time, the enzyme's overall activity decreased significantly with increasing cardenolide resistance and only the least substituted mimic of the Na,K-ATPase α1C copy maintained activity similar to the wild-type enzyme. Our results suggest that the Na,K-ATPase copies in O. fasciatus have diverged in function, enabling specific adaptations to dietary cardenolides while maintaining the functionality of this critical ion carrier.
Molecular Evolutionary Biology, Zoological Institute, Biocenter Grindel, University of Hamburg, 20146, Hamburg, Germany.
Safaa
S
Dalla
Molecular Evolutionary Biology, Zoological Institute, Biocenter Grindel, University of Hamburg, 20146, Hamburg, Germany.
Susanne
S
Dobler
D000220:Adaptation, Biological; D019943:Amino Acid Substitution; D000818:Animals; D000898:Antibiosis; D031108:Asclepias / Q000737:chemistry; D002298:Cardenolides / Q000378:metabolism*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics / Q000378:metabolism; D020440:Gene Duplication; D060434:Herbivory; D020062:Heteroptera / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D017422:Sequence Analysis, DNA; D000254:Sodium-Potassium-Exchanging ATPase / Q000235:genetics* / Q000378:metabolism
D002298:Cardenolides; D029721:Drosophila Proteins; C472021:ATPalpha protein, Drosophila; D000254:Sodium-Potassium-Exchanging ATPase
Coevolutionary interactions; Na,K-ATPase; Oncopeltus fasciatus; functional trade-off; plant-herbivore interactions; target site insensitivity