Voltage-gated ion channel TRP/Painless regulates the excretory function of the Malpighian tubules in larval lepidopterans

Abstract

Lepidopteran larvae are agricultural pests that feed voraciously and grow rapidly, requiring an efficient excretory system, consisting of a combination functionally equivalent to the human kidney - Malpighian tubules (MTs) and hindgut. In larval lepidopterans, distal ends of MTs are embedded into a specialized organ termed the rectal complex, enabling dietary extraction of ions and water, which drives fluid secretion and excretion in their MTs. A unique feature of caterpillar MTs is that they can rapidly (∼10 min) switch between using haemolymph ions and dietary ions to maintain constant fluid secretion in the face of changing dietary ion availability. Previous transcriptomic studies suggested that voltage-gated ion channels (VGICs) are expressed in the MTs of the larval cabbage looper Trichoplusia ni, providing the basis for one of the mechanisms enabling this rapid ion transport switch. In the current study, we demonstrate that Ca2+-permeable TRP/Painless (and other VGICs) are expressed in the DIP of Trichoplusia ni, Bombyx mori, Manduca sexta, Plutella xylostella and Spodoptera frugiperda larvae. In larval T. ni, we demonstrate that TRP/Painless is found in the secondary cells of the distal ileac plexus (DIP) and its mRNA abundance is higher in the secreting DIP. Moreover, pharmacological inhibition of TRP/Painless reduces transepithelial membrane potential, K+ transport by principal cells and fluid secretion rate, while TRP/Painless activation does the opposite. Our data demonstrate that TRP/Painless regulates ion transport in epithelia of lepidopteran MTs. This work may provide targets for future integrated pest management strategies aimed specifically at lepidopteran larvae in the agricultural setting.

Keywords: Ion transport; Malpighian tubule; Secondary cells; Voltage-gated ion channels.