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First published online December 15, 2004
Journal of Experimental Biology 208, vi (2005)
Copyright © 2005 The Company of Biologists Limited
doi: 10.1242/jeb.01392

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PERITROPHIC ENVELOPE IS CANNON FODDER

Art Woods

The University of Texas at Austin

art.woods{at}mail.utexas.edu

Topologically speaking, insects are ring donuts. The gut is therefore an important point of contact between insects and the plants they eat, and is where much of the cloak-and-dagger intrigue between plants and insects is played out. One devious plant strategy is to foment the formation of free radicals inside its adversary. Free radicals lead to a host of ills via the damage they inflict on diverse classes of molecules. Some of the most reactive - hydroxyl and alkoxyl radicals - are formed when common constituents of gut fluid occur together with a suitable catalyst, such as ferrous iron ions. This chemical potential has not gone unnoticed by plants. Many contain enough iron in their tissues to trigger free radical formation in insects' guts, attacking their foes from the inside out. What's an insect on an iron-rich diet to do?

Raymond Barbehenn and Jasmine Stannard recently tested the hypothesis that insects protect themselves from free radicals by placing the peritrophic envelope in the line of fire. The envelope surrounds the gut contents like a leaky glove. It is secreted by cells at the foregut-midgut junction, is carried along by movement of food in the gut tract, and eventually is excreted. Orthodox thinking says that the peritrophic envelope protects gut cells from abrasion while still letting through digested nutrients. Could it also protect insects from an onslaught of free radicals?

To find out, the team first fed Malacosoma disstria caterpillars artificial diets containing low, medium, or high amounts of iron, and then removed the caterpillars' peritrophic envelopes and analyzed them for iron content. They found, as suspected, that envelopes scavenge iron. The next step was to test whether the peritrophic envelope protects midgut tissue from oxidative damage. The researchers spiked diets with radical-producing compounds (tannins) and different levels of iron, and then measured damage to proteins in midgut tissue. The level of iron made no difference; midgut tissues were protected even from high-iron diets. Finally, the team examined whether the peritrophic envelope itself takes the fall, by feeding caterpillars tannin or no-tannin diets, both containing iron. They found that envelope proteins from caterpillars eating tannins sustained about twice the oxidative damage as those in caterpillars fed no-tannin diets. Barbehenn and Stannard's findings suggest that the peritrophic envelope both prevents iron from reaching midgut tissues and absorbs the free radicals catalyzed by iron. The disposable envelope thus takes the oxidative fall for the more permanent and highly active midgut epithelium.

A curmudgeon could object that these experiments do not definitively rule out a primary role for other systems that protect from free radicals. Barbehenn and Stannard pre-empt such criticisms with an elegant peritrophic envelope disruption experiment. They fed caterpillars a diet containing both tannin and Calcoflour, which disrupts peritrophic envelope structure. Caterpillars receiving this experimental diet had two- to three-fold higher levels of oxidative damage in their midgut tissue than caterpillars fed control diets. The peritrophic envelope indeed appears to be a primary system protecting midgut tissues from free radical damage.

The simple view of peritrophic envelope function - that it protects the midgut from abrasion - is increasingly dated. An emerging multifunctional view emphasizes the envelope's multiple roles in digestion and its ability to alter chemical conditions in the gut to the insect's advantage. In the baroque and interlocking battle between insects and plants, the peritrophic envelope now appears to be a central player.

References