The rectal complex and Malpighian tubules of the cabbage looper (Trichoplusia ni): regional variations in Na+ and K+ transport and cation reabsorption by secondary cells

Abstract

In larvae of most Lepidoptera the distal ends of the Malpighian tubules are closely applied to the rectal epithelia and are ensheathed within the perinephric membrane, thus forming the rectal complex. The cryptonephric Malpighian tubules within the rectal complex are bathed in fluid within a functional compartment, the perinephric space, which is separate from the haemolymph. In this study, the scanning ion-selective electrode technique (SIET) was used to measure transport of Na + and K + across the rectal complex and across multiple regions of the Malpighian tubules of larvae of the cabbage looper Trichoplusia ni. Measurements were made in an intact preparation in which connections of the tubules upstream to the rectal complex and downstream to the urinary bladder and gut remained intact. SIET measurements revealed reabsorption of Na + and K + across the intact rectal complex and into the bath (haemolymph), with K + fluxes approximately twice as large as those of Na + . Analyses of fluxes in larvae with empty guts, found in recently moulted larvae, versus those with full guts highlighted differences in the rates of K + or Na + transport within tubule regions that appeared morphologically homogeneous, such as the rectal lead. The distal rectal lead of larvae with empty guts reabsorbed K + , whereas the same region secreted K + in tubules of larvae with full guts. SIET measurements of the ileac plexus also indicated a novel role for secondary (type II) cells in cation reabsorption. Secondary cells reabsorb K + , whereas the adjacent principal (type I) cells secrete K + . Na + is reabsorbed by both principal and secondary cells, but the rate of reabsorption by the secondary cells is approximately twice the rate in the adjacent principal cells.

Chilling induces unidirectional solute leak through the locust gut epithelia

“…Following the midgut are the MTs, blind-ended tube-shaped diverticula of the gut that are somewhat analogous to the vertebrate kidneys (Chapman, 2013). These tubules are one cell layer thick and contain a multitude of cation exchangers and pumps (Maddrell and O’Donnell, 1992; O’Donnell and Ruiz-Sanchez, 2015). Through these ionoregulatory pumps (e.g.…”

Calcium transport across the basolateral membrane of isolated Malpighian tubules: a survey of several insect orders

“…We find that Ca 2+ is taken up across only the principal cells of T. ni tubules. Although the secondary cells are sites of high rates of reabsorption of the monovalent cations Na + and K + (O'Donnell & Ruiz‐Sanchez, ), there is no evidence of reabsorption of the divalent cation Ca 2+ . There are several lines of evidence to suggest that Ca 2+ taken up by Malpighian tubules occurs specifically across principal cells.…”

“…As a result of the absence of available saline recipes for H. halys and P. occidentalis, Malpighian tubule dissections and experiments were performed in salines previously used to bathe Malpighian tubules from the related large milkweed bug Oncopeltus fasciatus (Te Brugge & Orchard, 2008), and the harvester ant Formica polyctena (Laenen et al, 2001), respectively. Procedures for the isolation of single Malpighian tubules have been described previously for A. aegypti (Scott et al, 2004), D. melanogaster (Browne & O'Donnell, 2016), A. domesticus (Browne & O'Donnell, 2017), T. molitor (Wiehart et al, 2002), P. americana (Kay et al, 1992) and T. ni (O'Donnell & Ruiz-Sanchez, 2015). Tubules of H. halys were dissected in accordance with a procedure similar to that used for O. fasciatus (Meredith et al, 1984).…”

Malpighian tubules ofTrichoplusia ni: recycling ions via gap junctions and switching between secretion and reabsorption of Na+ and K+ in the distal ileac plexus

“…Hardware, software and methodology for acquiring scanning ionselective electrode technique (SIET) data and calculating ion fluxes have been described in detail in previous publications (Donini and O'Donnell, 2005;O'Donnell and Ruiz-Sanchez, 2015). SIET was used to measure ion fluxes for isolated DIPs and also for the DIP in situ (i.e.…”

“…As shown in Fig. 1, larval lepidopterans demonstrate a so-called cryptonephric condition where the distal ends of the MTs are embedded into the rectal complex, juxtaposed to the rectal epithelium and bathed in fluid contained within the perinephric space which is separated from haemolymph by the enveloping perinephric membrane (Irvine, 1969;Ramsay, 1976;O'Donnell and Ruiz-Sanchez, 2015). Classic studies suggest that the primary function of the rectal complex in developing lepidopterans is to regulate the Na + /K + content of their haemolymph when presented with rapid changes due to the start and cessation of feeding (Ramsay, 1976).…”