Abstract
Phenylalanine hydroxylase (PAH) is a key tyrosine-biosynthetic enzyme involved in neurological and melanin-associated physiological processes. Despite extensive investigations in holometabolous insects, a PAH contribution to insect embryonic development has never been demonstrated. Here, we have characterized, for the first time, the PAH gene in a hemimetabolous insect, the aphid Acyrthosiphon pisum. Phylogenetic and sequence analyses confirmed that ApPAH is closely related to metazoan PAH, exhibiting the typical ACT regulatory and catalytic domains. Temporal expression patterns suggest that ApPAH has an important role in aphid developmental physiology, its mRNA levels peaking at the end of embryonic development. We used parental dsApPAH treatment to generate successful knockdown in aphid embryos and to study its developmental role. ApPAH inactivation shortens the adult aphid lifespan and considerably affects fecundity by diminishing the number of nymphs laid and impairing embryonic development, with newborn nymphs exhibiting severe morphological defects. Using single nymph HPLC analyses, we demonstrated a significant tyrosine deficiency and a consistent accumulation of the upstream tyrosine precursor, phenylalanine, in defective nymphs, thus confirming the RNAi-mediated disruption of PAH activity. This study provides first insights into the role of PAH in hemimetabolous insects and demonstrates that this metabolic gene is essential for insect embryonic development.
Highlights
Have been investigated in Drosophila, silkworms and mosquitoes[17,18,27,28,29,30,31,32], Phenylalanine hydroxylase (PAH) is associated with the numerous changes in cuticular coloration and sclerotization that allow for the extensive reconstruction and remodeling of internal structures occurring during metamorphosis
In many symbiotic insects that depend on their mutualistic prokaryotic partners for the production of essential nutrients, such as vitamins or amino acids, convergent evolution processes lead to strong host/symbiont collaboration for tyrosine biosynthesis: symbionts supply the insect with tyrosine metabolic precursors which the host transforms into tyrosine[45,46]
Tyrosine metabolism in the A. pisum/B. aphidicola symbiotic system is a striking example and can be considered as a model for mutual metabolic interdependence, consisting of an integrated network of genes encoded by both partner genomes[36,47,48]
Summary
Have been investigated in Drosophila, silkworms and mosquitoes[17,18,27,28,29,30,31,32], PAH is associated with the numerous changes in cuticular coloration and sclerotization that allow for the extensive reconstruction and remodeling of internal structures occurring during metamorphosis. We have identified tyrosine biosynthesis as a key metabolic pathway for parthenogenetic development of the pea aphid Acyrthosiphon pisum[34], a major globally distributed crop pest This emerging model organism, whose genome was the first to be sequenced and annotated among the hemimetabolous insects[35], provides unique opportunities for the study of genetic mechanisms regulating its embryonic development. The A. pisum PAH putative gene (ACYPI007803), which belongs to the highly expressed gene group, shows significantly increased expression levels in late embryos and in the first nymphal stage Consistent with this gene regulation, HPLC analyses have shown that tyrosine accumulates throughout embryonic development, supporting the hypothesis of a key function for the PAH enzyme, and its amino acid product, in the terminal phase of aphid embryogenesis. We conclude that PAH is essential for insect embryonic development and reveal, for the first time, its key role in hemimetabolous insect physiology
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