Opposite Effects on Spodoptera littoralis Larvae of High Expression Level of a Trypsin Proteinase Inhibitor in Transgenic Plants

Abstract

This work illustrates potential adverse effects linked with the expression of proteinase inhibitor (PI) in plants used as a strategy to enhance pest resistance. Tobacco (Nicotiana tabacum L. cv Xanthi) and Arabidopsis [Heynh.] ecotype Wassilewskija) transgenic plants expressing the mustard trypsin PI 2 (MTI-2) at different levels were obtained. First-instar larvae of the Egyptian cotton worm (Spodoptera littoralis Boisd.) were fed on detached leaves of these plants. The high level of MTI-2 expression in leaves had deleterious effects on larvae, causing mortality and decreasing mean larval weight, and was correlated with a decrease in the leaf surface eaten. However, larvae fed leaves from plants expressing MTI-2 at the low expression level did not show increased mortality, but a net gain in weight and a faster development compared with control larvae. The low MTI-2 expression level also resulted in increased leaf damage. These observations are correlated with the differential expression of digestive proteinases in the larval gut; overexpression of existing proteinases on low-MTI-2-expression level plants and induction of new proteinases on high-MTI-2-expression level plants. These results emphasize the critical need for the development of a PI-based defense strategy for plants obtaining the appropriate PI-expression level relative to the pest's sensitivity threshold to that PI.

Potential Use of a Serpin from Arabidopsis for Pest Control

“…Serine proteases provide the major midgut endoproteolytic activities in S. littoralis larvae [34], and previous studies have demonstrated that transgenic plants expressing serine protease inhibitors can confer resistance against S. littoralis [45], [46]. When the protease inhibitor AtSerpin1 was incorporated into an artificial diet, the weight gain of S. littoralis larvae was substantially reduced relative to the control.…”

Proteinase inhibitors and their function in plants: A review

“…The main reason for such observations is the presence in phytophagous insects of a variety of mechanisms that counter adverse effects of plant proteinase inhibitors. The simplest mechanism involves increasing the secretion of the proteinase sensitive to the inhibitor [316]. Alternatively, the inhibitor may be cleaved by those intestinal proteinases that are resistant to it [317,318].…”

Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defence protease inhibitor

“…Available molecular and biochemical studies have revealed several diverse strategies used by insect herbivores. They may (1) overproduce the existing digestive enzymes to ‘titre out’ the inhibitors (De Leo et al ., 1998); (2) express different enzymes, which are insensitive to the protease inhibitors (Bolter & Jongsma, 1995; Jongsma et al ., 1995; Bown et al ., 1997; Cloutier et al ., 2000; Mazumdar‐Leighton & Broadway, 2001); or (3) activate expression of hydrolysing enzymes that fragment the inhibitors (Michaud et al ., 1995; Giri et al ., 1998). Cowpea bruchids apparently are able to employ all three of these strategies when challenged by dietary scN at a dosage level equivalent to the natural plant defence response when attacked by insect herbivores (Zhu‐Salzman et al ., 2003).…”