Abstract
Cuticle renewal is a complex biological process that depends on the cross talk between hormone levels and gene expression. This study characterized the expression of two genes encoding cuticle proteins sharing the four conserved amino acid blocks of the Tweedle family, AmelTwdl1 and AmelTwdl2, and a gene encoding a cuticle peroxidase containing the Animal haem peroxidase domain, Ampxd, in the honey bee. Gene sequencing and annotation validated the formerly predicted tweedle genes, and revealed a novel gene, Ampxd, in the honey bee genome. Expression of these genes was studied in the context of the ecdysteroid-coordinated pupal-to-adult molt, and in different tissues. Higher transcript levels were detected in the integument after the ecdysteroid peak that induces apolysis, coinciding with the synthesis and deposition of the adult exoskeleton and its early differentiation. The effect of this hormone was confirmed in vivo by tying a ligature between the thorax and abdomen of early pupae to prevent the abdominal integument from coming in contact with ecdysteroids released from the prothoracic gland. This procedure impaired the natural increase in transcript levels in the abdominal integument. Both tweedle genes were expressed at higher levels in the empty gut than in the thoracic integument and trachea of pharate adults. In contrast, Ampxd transcripts were found in higher levels in the thoracic integument and trachea than in the gut. Together, the data strongly suggest that these three genes play roles in ecdysteroid-dependent exoskeleton construction and differentiation and also point to a possible role for the two tweedle genes in the formation of the cuticle (peritrophic membrane) that internally lines the gut.
Highlights
Insects grow and differentiate from the larval to the adult stage through periodic degradation of the exoskeleton and replacement by a new one
This cyclic re-construction of the cuticle is a complex task involving the expression of genes for extensive synthesis of structural cuticle proteins (CPs) and enzymes with roles in cuticle pigmentation and sclerotization
Molting initiation is ensured by the increase in ecdysteroid titer, but the synthesis of a new cuticle and ecdysis only take place when the titer of ecdysteroids decreases after the peak [28,29,30,31]
Summary
Insects grow and differentiate from the larval to the adult stage through periodic degradation of the exoskeleton (or cuticle) and replacement by a new one. Each episode of cuticle renewal, or molt, comprises a series of events mainly marked by the detachment of the cuticle from the subjacent epidermis (apolysis), the synthesis and secretion of the components of the new cuticle by the epidermal cells, and the ecdysis or shedding of the old cuticle [1] This cyclic re-construction of the cuticle is a complex task involving the expression of genes for extensive synthesis of structural cuticle proteins (CPs) and enzymes with roles in cuticle pigmentation (darkening) and sclerotization (hardening). Data from Manduca sexta have been used to construct a proposed neuroendocrine model for the regulation of molting events that may apply to insects in general According to this model, the increase in ecdysteroid levels that induces apolysis and early gene expression concomitantly makes the insect central nervous system (CNS) sensitive to the pre-ecdysis hormone and ecdysis-triggering hormone produced by the tracheal Inka cells. This sequence of events triggered and timed by ecdysteroids, which includes many other molecular components in addition to those mentioned above, underlies the process of cuticle renewal
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