Novel mechanisms of epithelial ion transport: insights from the cryptonephridial system of lepidopteran larvae

Lepidopterans are among the most widespread and easily recognized insects. Whereas adult lepidopterans are known for their beauty and ecological importance as pollinators and sources of food for other animals, larvae are economically important pests of forests and agricultural crops. In the larval body, rapid growth while feeding on plant-based diet is associated with extreme alkalinity (up to pH = 11) of the midgut lumen that helps digest plant proteins. Additionally, the presence of plant secondary metabolites which serve as anti-herbivory agents requires uninterrupted excretory function, accomplished primarily by the Malpighian tubules (MTs). The so-called cryptonephridial condition, along with extreme regional heterogeneity of the MTs, and the ability to rapidly and reversibly alter the direction of epithelial ion transport are features that allow uninterrupted MT functioning and recycling of base equivalents. Studies of MTs in lepidopteran larvae have revealed that rapid adjustments in epithelial ion transport include unexpected roles for voltage-gated, ligand-gated and mechanosensitive ion channels, as well as gap junctions. These molecular components are present in epithelia of a variety of vertebrates and invertebrates and thus are likely to constitute a universal epithelial toolkit for rapid autonomous regulation of epithelial function.