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GABA, β-Alanine and Glycine in the Digestive Juice of Privet-Specialist Insects: Convergent Adaptive Traits Against Plant Iridoids

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Abstract

The privet tree, Ligustrum obtusifolium (Oleaceae), defends its leaves against insects with a strong lysine-decreasing activity that make proteins non-nutritive. This is caused by oleuropein, an iridoid glycoside. We previously found that some privet-specialist caterpillars adapt by secreting glycine in the digestive juice as a neutralizer that prevents the loss of lysine. Here, we extended the survey into 42 lepidopteran and hymenopteran species. The average concentration of glycine in digestive juice for 11 privet-feeding species (40.396 mM) was higher than that for 32 non-privet-feeding species (2.198 mM). The glycine concentrations exceeded 10 mM in 7 out of 11 privet-feeding species. In Macrophya timida (Hymenoptera), it reached 164.8 mM. Three out of the four remaining privet-feeding species had other amino acids instead. Larvae of a privet-specialist butterfly, Artopoetes pryeri (Lycaenidae), had a high concentration (60.812 mM) of GABA. In two other specialists, β-alanine was found. GABA, β-alanine, and glycine as well as alanine, amines, and ammonium ion inhibited the lysine decrease, indicating that amino residues are responsible for the inhibition. However, the three amino acids found in the specialists were far more effective (20 mM showed 80% inhibition) than the rest (>140 mM was required for 80% inhibition). Our results show a clear and rare case of the apparent convergent evolution of herbivores’ molecular adaptations of feeding on a plant with a chemical defense in a manner that minimizes the cost of adaptation. The novel role of GABA in plant-herbivore interactions shown here is probably the first reported non-neuronal role of animal-derived GABA.

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Acknowledgements

We thank Prof. Keiichi Honda in Hiroshima University for invaluable suggestions, and Mrs. Mayumi Hazeyama for rearing insects. This research was supported by the Enhancement of Center of Excellence, Special Coordination Funds for Promoting Science and Technology from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT), and by the Pioneer Research Project Fund from the Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF).

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Correspondence to Kotaro Konno.

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Konno, K., Hirayama, C., Yasui, H. et al. GABA, β-Alanine and Glycine in the Digestive Juice of Privet-Specialist Insects: Convergent Adaptive Traits Against Plant Iridoids. J Chem Ecol 36, 983–991 (2010). https://doi.org/10.1007/s10886-010-9842-y

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