Abstract
In tsetse flies, nutrients for intrauterine larval development are synthesized by the modified accessory gland (milk gland) and provided in mother's milk during lactation. Interference with at least two milk proteins has been shown to extend larval development and reduce fecundity. The goal of this study was to perform a comprehensive characterization of tsetse milk proteins using lactation-specific transcriptome/milk proteome analyses and to define functional role(s) for the milk proteins during lactation. Differential analysis of RNA-seq data from lactating and dry (non-lactating) females revealed enrichment of transcripts coding for protein synthesis machinery, lipid metabolism and secretory proteins during lactation. Among the genes induced during lactation were those encoding the previously identified milk proteins (milk gland proteins 1–3, transferrin and acid sphingomyelinase 1) and seven new genes (mgp4–10). The genes encoding mgp2–10 are organized on a 40 kb syntenic block in the tsetse genome, have similar exon-intron arrangements, and share regions of amino acid sequence similarity. Expression of mgp2–10 is female-specific and high during milk secretion. While knockdown of a single mgp failed to reduce fecundity, simultaneous knockdown of multiple variants reduced milk protein levels and lowered fecundity. The genomic localization, gene structure similarities, and functional redundancy of MGP2–10 suggest that they constitute a novel highly divergent protein family. Our data indicates that MGP2–10 function both as the primary amino acid resource for the developing larva and in the maintenance of milk homeostasis, similar to the function of the mammalian casein family of milk proteins. This study underscores the dynamic nature of the lactation cycle and identifies a novel family of lactation-specific proteins, unique to Glossina sp., that are essential to larval development. The specificity of MGP2–10 to tsetse and their critical role during lactation suggests that these proteins may be an excellent target for tsetse-specific population control approaches.
Highlights
Tsetse reproductive biology is unusual among insects
Identification of genes associated with lactation by transcriptome analyses To understand the major products of lactation and factors that may be responsible for regulating their expression, we analyzed two RNA-seq libraries
Distribution of reads per contig was comparable between the two datasets with the exception that there was a greater number of highly expressed genes in lactating flies (Fig. S2)
Summary
Tsetse reproductive biology is unusual among insects. Female tsetse give birth to a fully mature third instar larva (viviparity) after an extended intrauterine gestation. This reproductive strategy limits the capacity of tsetse mothers to only 8–10 offspring per lifetime [1]. To accommodate intrauterine larval development, the morphology and physiology of the female tsetse reproductive organs have undergone extensive modification. The reproductive tract has been expanded into a uterus to serve as a safe harbor for developing larvae. The female accessory gland has been modified and expanded to provide milk that is secreted into the uterus and consumed by the developing larva [1]. Identification of factors specific to milk production could lead to development of novel tsetse-specific compounds that interfere with larval development and induce abortion (abortifacients) without impacting non-target insects
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