Control of the release of digestive enzymes in the larvae of the fall armyworm, Spodoptera frugiperda

Abstract

There is a basal level of enzyme activity for trypsin, aminopeptidase, amylase, and lipase in the gut of unfed larval (L6) Spodoptera frugiperda. Trypsin activity does not decrease with non-feeding, possibly because of the low protein levels in plants along with high amino acid requirements for growth and storage (for later reproduction in adults). Therefore, trypsin must always be present so that only a minimal protein loss via egestion occurs. Larvae, however, adjust amylase activity to carbohydrate ingestion, and indeed amylase activity is five-fold higher in fed larvae compared to unfed larvae. Gut lipase activity is low, typical of insects with a high carbohydrate diet. A flat-sheet preparation of the ventriculus was used to measure the release of enzymes in response to specific nutrients and known brain/gut hormones in S. frugiperda. Sugars greatly increase (>300%) amylase release, but starch has no effect. Proteins and amino acids have little or no effect on trypsin or aminopeptidase release. The control of enzyme release in response to food is likely mediated through neurohormones. Indeed, an allatostatin (Spofr-AS A5) inhibits amylase and trypsin, and allatotropin (Manse- AT) stimulates amylase and trypsin release. Spofr-AS A5 also inhibits ileum myoactivity and Manse-AT stimulates myoactivity. The epithelial secretion rate of amylase and trypsin was about 20% of the amount of enzyme present in the ventricular lumen, which, considering the efficient counter-current recycling of enzymes, suggests that the secretion rate is adequate to replace egested enzymes.

Peptidergic control of food intake and digestion in insects1This review is part of a virtual symposium on recent advances in understanding a variety of complex regulatory processes in insect physiology and endocrinology, including development, metabolism, cold hardiness, food intake and digestion, and diuresis, through the use of omics technologies in the postgenomic era.

“…FGLa/AST immunoreactivity was also observed in all ganglia of the CNS and within the open-type endocrine cells in midguts of L. migratoria (Robertson and Lange 2010) and the Pacific beetle cockroach (Diploptera punctata (Eschscholtz, 1822)) (Reichwald et al 1994). In addition, some regulatory peptides show stimulatory or inhibitory effects on enzyme activity levels in the gut, indicating that the control of enzyme release in response to food is likely (at least partially) mediated through these neuropeptides (Harshini et al 2002(Harshini et al , 2003Woodring et al 2009;Lwalaba et al 2010). The following sections provide an overview of neuropeptides associated with the SNS and (or) endocrine cells in the midgut and thus potentially involved in control of feeding and digestion mechanisms in insects.…”

“…In contrast to this, in larvae of the lepidopteran fall armyworm (Spodoptera frugiperda (J.E. Smith, 1797)), AST-A5 inhibits amylase and trypsin release (Lwalaba et al 2010). In addition, FGLa/AST also influences the carbohydrase levels in the cockroach midgut.…”

“…The physiology of the insect digestive system is largely coordinated by neurohormones, as well as by multiple regulatory peptides produced by endocrine cells located in the gut epithelium and (or) by neurons innervating different parts of the gut (reviewed by Audsley and Weaver 2009;Woodring et al 2009;Lwalaba et al 2010). Many of these regulatory peptides in insects have vertebrate homologues; however, much less is known about their specific functions or modes of action in invertebrates.…”

“…Some neuropeptides present in the stomatogastric nervous system (SNS) have indeed also been localized in the midgut endocrine cells, suggesting a more prominent role in the regulation of digestive processes as well. In addition, some regulatory neuropeptides show stimulating or inhibitory effects on enzyme activity levels in the gut of insects, indicating that the control of enzyme release in response to food is likely to be (at least in part) under neuropeptidergic control (Harshini et al 2002(Harshini et al , 2003Woodring et al 2009;Lwalaba et al 2010). Understanding the endocrine control of digestion and feeding mechanisms is important in understanding the physiology of nutrition.…”

Families of allatoregulator sequences: a 2011 perspective1This review is part of a virtual symposium on recent advances in understanding a variety of complex regulatory processes in insect physiology and endocrinology, including development, metabolism, cold hardiness, food intake and digestion, and diuresis, through the use of omics technologies in the postgenomic era.

“…This finding suggested that Manse-AT has alternate functions. These activities include acting as a cardioaccelerator (Veenstra et al 1994;Koladich et al 2002a); a stimulator of ventral diaphram oscillations (Koladich et al 2002b); a stimulator opposing Manse-ASTinduced inhibition of foregut contraction in cotton bollworm (Helicoverpa armigera (Hübner, 1805)) and L. oleracea (Duve et al 1999;Matthews et al 2007); a stimulator of gut amylase and trypsin secretion and ileum contraction in opposition to Spofr-PISCF/AST (Lwalaba et al 2010); an inhibitor of ion exchange across the midgut epithelium (Lee et al 1998); and a regulator of photic entrainment of the circadian clock (Würden and Homberg 1995;Petri et al 2002). The pleiotropic functions ascribed to this peptide family may account for their presence in the genomes of Crustacea (Christie et al 2011;Dircksen et al 2011), molluscs (Veenstra 2010), and annelids (Veenstra 2011).…”