Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores

Abstract

The rate of hydrolysis of the abundant foliar protein, ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPC), in enzymatically active gut fluid ofManduca sexta larvae is very rapid and is unaffected by the presence of tannic acid, even when tannic acid is present in the incubation mixture in amounts in excess of the amount of RuBPC. When this protein is dissolved in the denatured gut fluids ofM. sexta larvae orSchistocerca gregaria nymphs, large amounts of tannic acid must be added to bring about the precipitation of significant quantities of protein. The ability of insect gut fluid to prevent the formation of insoluble tannin-protein complexes is due to the presence of surfactants. On the basis of our results and a review of the findings of other investigators, we argue that there is no evidence that tannins reduce the nutritional value of an insect's food by inhibiting digestive enzymes or by reducing the digestibility of ingested proteins and, further, that the failure of tannins to interfere with digestion is readily explained on the basis of well-documented characteristics of the digestive systems of herbivorous insects. In challenging the currently popular notion that tannins are digestibility-reducing substances, we do not challenge the general utility of either the apparency theory or resource availability theory of plant defense. In debating the merits of these two analyses of plant-herbivore interactions, however, the demise of tannins as all-purpose, dose-dependent, digestibility-reducing defensive substances must be taken into account.

Divergence in Structure and Activity of Phenolic Defenses in Young Leaves of Two Co-Occurring Inga Species

“…The "tannin-protein binding" mode of action has been questioned since (1) the guts of many herbivorous lepidoptera, with their high pHs and detergent content, are well adapted to prevent formation of polyphenol/protein complexes (Martin and Martin, 1984;Blytt et al, 1988), and (2) this mechanism has never been demonstrated in vivo. Martin et al (1987) showed that in Manduca sexta gut fluid hydrolyzable tannin-RUBISCO ratios must be at unity or greater for appreciable protein precipitation to occur. They suggest that such high polyphenol/protein ratios would only rarely be encountered in nature, and that protein precipitation is, therefore, probably not an ecologically relevant process.…”

Cowpea Chloroplastic ATP Synthase Is the Source of Multiple Plant Defense Elicitors during Insect Herbivory

“…Within 15 min of completed GSTGmIn8H consumption by the larvae (defined as time zero), 80% of the total potential inceptin-like peptides present within the diet were recovered in the OS as active elicitors. Similarly, gut fluids of hornworm (Manduca sexta) larvae are known to efficiently proteolyze 100% of precipitable Rubisco within this same period (Martin et al, 1987). The midguts of armyworm harbor potent trypsin and chymotrypsin endopeptidase activities; thus, Lys and Phe cleavage sites near the termini of the Gm-In ( 1 KGEICDVNGVCVDAAEDEF 2 ) are predicted to facilitate this process (Keil, 1992;Paulillo et al, 2000).…”

Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees

“…For example, the principal role of tannins traditionally has been thought to be the precipitation of proteins via hydrogen bonding. Although this might occur under certain conditions, such a mechanism is ineffective against some insect herbivores, many of which have alkaline midgut and/or surfactants in their gut fluid; these prevent the formation of insoluble protein-tannin complexes (Martin et al 1987, Appel 1993. However, at high pH (e.g.…”