Abstract
BackgroundPhytophagous insects have emerged successfully on the planet also because of the development of diverse and often astonishing defensive strategies against their enemies. The larvae of the mustard leaf beetle Phaedon cochleariae, for example, secrete deterrents from specialized defensive glands on their back. The secretion process involves ATP-binding cassette transporters. Therefore, sugar as one of the major energy sources to fuel the ATP synthesis for the cellular metabolism and transport processes, has to be present in the defensive glands. However, the role of sugar transporters for the production of defensive secretions was not addressed until now.ResultsTo identify sugar transporters in P. cochleariae, a transcript catalogue was created by Illumina sequencing of cDNA libraries. A total of 68,667 transcripts were identified and 68 proteins were annotated as either members of the solute carrier 2 (SLC2) family or trehalose transporters. Phylogenetic analyses revealed an extension of the mammalian GLUT6/8 class in insects as well as one group of transporters exhibiting distinctive conserved motifs only present in the insect order Coleoptera. RNA-seq data of samples derived from the defensive glands revealed six transcripts encoding sugar transporters with more than 3,000 counts. Two of them are exclusively expressed in the glandular tissue. Reduction in secretions production was accomplished by silencing two of four selected transporters. RNA-seq experiments of transporter-silenced larvae showed the down-regulation of the silenced transporter but concurrently the up-regulation of other SLC2 transporters suggesting an adaptive system to maintain sugar homeostasis in the defensive glands.ConclusionWe provide the first comprehensive phylogenetic study of the SLC2 family in a phytophagous beetle species. RNAi and RNA-seq experiments underline the importance of SLC2 transporters in defensive glands to achieve a chemical defense for successful competitive interaction in natural ecosystems.
Highlights
Except for SCRT, which was classified as a member of family 49 of solute carriers (SLCs) [17], they all belong to the solute carrier 2 (SLC2) family of glucose and polyol transporters [24,25,26,27]
In order to predict sugar transporters in the larvae of P. cochleariae with special emphasis on the defensive glands, we performed a comprehensive analysis of transcriptomic data
In addition to the sequencing of cDNA derived from a tissue pool in 150 bp paired-end mode, three biological replicates of the RNA of P. cochleariae’s defensive glands were extracted, processed and each sequenced in 50 bp single-read modes
Summary
For glucose absorption in the mammalian small intestine two pathways are known: the passive, paracellular absorption which bats rely on for more than 70% of their total sugar uptake [1] and the transporter-mediated transcellular pathways which non-flying mammals use preferentially. They take up glucose from interstitial fluid by a passive, facilitative transport process driven by the downward concentration gradient across the plasma membrane [2]. Sugar as one of the major energy sources to fuel the ATP synthesis for the cellular metabolism and transport processes, has to be present in the defensive glands. The role of sugar transporters for the production of defensive secretions was not addressed until now
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