Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases

Protease inhibitors have been proposed as potential control molecules that could be engineered into potato plants for developing crops resistant to th e Colorado potato beetle, Leptinotarsa decemlineata, a major pest of potato and other Solanaceae. In this study, we examined the effects of feeding yo ung female beetles with foliage from a cultivar of the "Kennebed' potato li ne (K52) transformed with a gene encoding oryzacystatin I (OCI), a specific cysteine proteinase inhibitor with proven activity against cathepsin H-lik e enzymes of larvae and adults of the potato beetle. To evaluate the insect 's performance, we collected data over a 16-d postemergence period on survi val, diapause incidence, foliage consumption, weight gain, and oviposition of females. Tested individuals were fed untransformed (control) and OCI-tra nsformed foliage at two stages of potato leaf differentiation, correspondin g to 'low" and "high" levels of OCI expression in leaves of K52. The OCI-ex pressing foliage did not affect female survival (close to 100%), incidence of diapause (15-30%), relative growth rate (RGR) during postemergence growt h (5-9% d(-1)) or maximum weight reached (140-160 mg). Neither did it affec t female reproductive fitness as measured by preoviposition time (8-9 d), 1 6-d fecundity (220-290 eggs), or egg eclosion incidence (86-91%). However, nutritional stress to females feeding on OCI foliage was evident, as reflec ted in their lower efficiency of conversion of ingested foliage (ECI) durin g postemergence growth, increased foliage consumed per egg laid (up to 119% more), and adaptation of their digestive proteolytic system to the inhibit ory effect of OCI. Interestingly, beetles fed foliage expressing the highes t level of OCI reacted rapidly to the presence of OCI by producing OCI-inse nsitive proteases, and exhibiting strong hypertrophic behavior by ingestion of 2.4-2.5 times more OCI rich foliage apparently as a compensatory respon se for nutritional stress due to the protease inhibitor in their diet. Arch . Insect Biochem. Physiol. 44:69-81, 2000. (C) 2000 Wiley-Liss, Inc.