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

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.

How insects overcome two‐component plant chemical defence: plant β‐glucosidases as the main target for herbivore adaptation

“…In addition to the various adaptations that often target plant β‐glucosidase activity, single amino acids were shown to counteract activity of plant β‐glucosidases mainly by reducing the toxicity of released aglucones. Several lepidopteran and hymenopteran larvae secrete extraordinarily high amounts of glycine, β‐alanine or γ‐aminobutyric acid (GABA) into their gut lumen when feeding on plants containing the iridoid glucoside oleuropein (Konno et al , , , ; Konno, Okada & Hirayama, ). These single amino acids protect insect digestive enzymes and dietary protein by competing with the amino residue in the lysine side chains of proteins for the protein‐crosslinking activity of aglucones (Konno et al , ).…”

“…Several lepidopteran and hymenopteran larvae secrete extraordinarily high amounts of glycine, β‐alanine or γ‐aminobutyric acid (GABA) into their gut lumen when feeding on plants containing the iridoid glucoside oleuropein (Konno et al , , , ; Konno, Okada & Hirayama, ). These single amino acids protect insect digestive enzymes and dietary protein by competing with the amino residue in the lysine side chains of proteins for the protein‐crosslinking activity of aglucones (Konno et al , ). Leaves of the privet tree are defended by oleuropein, but larvae of the lepidopteran Brahmaea wallichii (Brahmaeidae) and Dolbina tancrei (Sphingidae) or the hymenopteran Macrophya timida (Tenthredinidae) can feed on this plant by secreting extremely high concentrations of free glycine (up to 164 mM) into their midgut (Konno et al , , ).…”

“…These single amino acids protect insect digestive enzymes and dietary protein by competing with the amino residue in the lysine side chains of proteins for the protein‐crosslinking activity of aglucones (Konno et al , ). Leaves of the privet tree are defended by oleuropein, but larvae of the lepidopteran Brahmaea wallichii (Brahmaeidae) and Dolbina tancrei (Sphingidae) or the hymenopteran Macrophya timida (Tenthredinidae) can feed on this plant by secreting extremely high concentrations of free glycine (up to 164 mM) into their midgut (Konno et al , , ). This is more than 20‐fold higher than seen in non‐privet feeders (Konno et al , ).…”

Deciphering the route to cyclic monoterpenes in Chrysomelina leaf beetles: source of new biocatalysts for industrial application?

“…If the resulting compound is a reactive aldehyde, it has the ability to link irreversibly and nonselectively essential cellular components including proteins. This may affect the physiological processes of invasive organisms directly and/or decrease the nutritive value of dietary proteins considerably [25][26][27][28]. Although a universal target of iridoids has not been defined, these rather nonspecific effects contribute to an increased mortality of, for example, nonadapted herbivores feeding on iridoid glycoside-containing diets [24].…”

Impact of the dual defence system of Plantago lanceolata (Plantaginaceae) on performance, nutrient utilisation and feeding choice behaviour of Amata mogadorensis larvae (Lepidoptera, Erebidae)

“…Hydrolysed iridoid glycosides can interfere with the assimilation of nutrients and in particular with that of dietary nitrogen (Konno et al, 2010;Konno et al, 1998). As growth rates of herbivorous insects depend on a proper balance of nutrients (Behmer, 2009) and mainly correlate to the nitrogen content of the food (Coley et al, 2006), secondary plant compounds that interfere with the availability of dietary nitrogen should therefore negatively affect herbivore performance.…”