Of the nature of insecticidal proteins and their anticipated ecological effects

The novelty and nature of insecticidal proteins dictate a case-by-case problem formulation for ecological safety. Problem formulation is used to structure a plan for characterizing effects and exposure. History of safe use of a protein or its close analogs is another important criterion for formulation of the risk assessment. For future plant transgenic proteins, the process of problem formulation will be similar to that described here for currently commercial products, even though the outcome — the structure of effects and exposure characterization needed for the ecological safety determination — may differ. The problem formulation should consider mode of action, spectrum of bioactivity, and characterization of the protein expressed in the plant in arriving at an appropriate analysis plan.

For the Cry proteins, knowledge of their activity and selectivity in plants largely relies on the vast body of literature characterizing the mode of action and activity of biopesticides originating from B. thuringiensis?A These pesticides, formulated as sprays, have proven to be of no toxicological concern for birds, fish, mammals, and nonherbivorous arthropods, and they have a long-established history of safe use.

The insecticidal properties of B. thuringiensis were described as early as 1901,3536 and cultured Bts were first used as sprayable insecticides in the 1950s.35 Classification systems describe numerous subspecies of Bt on the basis of flagella antigen serotype37 as well as their crystalline proteins.38 The distribution of subspecies is relatively uniform throughout the world.39 Although particular isolates of Bt may exhibit differing suites of protein conferring insecticidal activity (8-endotoxins), they are readily transferable among subspecies through plasmid transmission.40 Therefore, the 8-endotoxins are generally considered environmentally ubiquitous. Even Cry proteins with novel and recently discovered insecticidal activity (e.g., Cry34Abl/Cry35Abl) are commonly distributed in nature, along with more familiar Cry proteins.4l

Naturally occurring Bt 8-endotoxins are in the form of protoxins. Insecticidal activity is conveyed when the ingested protoxin undergoes proteolysis in the insect gut to form toxic polypeptides.42 Previous research on sprayable Bt indicates that specific pH levels, enzymes, and gut receptors are required for solubility, activation, and binding of the 8-endotoxins.43 Isolation of a specific cry gene coding for a 8-endotoxin, coupled with recombinant techniques and gene insertion technology, gives rise to genetically engineered crops expressing Cry protein. Gene optimization and transformation techniques allowing for insertion into the host plant genome cause toxin expression in the plant in forms closely resembling the processed natural and sprayable protein. Depending on the specific event considered, the transgenically produced protein may vary from full-length protoxin to partially or fully processed toxin. Trends in the development of modern sprayable Bt formulations as well as Bt crops are for increased activity, specificity, purity, and stability of the 8-endotoxin.35 A Bt isolate was first registered in the United States for commercial use in 1961.40 Within the United States, isolates of Bt have a wide variety of agricultural and non-agricultural uses.

The activity of Cry proteins is restricted to specific herbivorous insect species within a given order (Lepidoptera, Coleoptera, Diptera, and Orthoptera),34 or nematodes in the case of Cry5 proteins.10 Susceptibility data help to confirm the reported spectrum of activity for insecticidal proteins. For instance, in the case of the Cryl proteins, the greatest activity is shown for the order Lepidoptera,44 which is confirmed for specific Cryl proteins through the conduct of selectivity studies using microbially derived proteins to establish the spectrum of activity against a suite of insect pests.45

Even if susceptible to Cry proteins, organisms not directly feeding on transgenic plant materials are unlikely to be exposed to these proteins.46 Therefore, because of lack of susceptibility and exposure, large margins of safety are shown in the literature for nontarget terrestrial and aquatic species. Current evidence suggests that Cry proteins have activity against only holometabolous insects.34 On this basis, problem formulation anticipates that toxicity for currently commercialized plant insecticidal proteins (various Cry proteins) will be restricted primarily to classes of insects that are the targets for pest control. Therefore, nontarget insects representative of sensitive groups, and with environmentally relevant exposure routes, should garner the closest scrutiny in risk assessment. In the parlance of risk assessment, these nontarget organisms are deemed "ecological entities of concern." In addition, for the purposes of regulatory assessments, a spectrum of vertebrate or invertebrate species other than specific entities of concern are frequently considered in risk characterization. This is done to confirm the general spectrum of activity for a given protein. Finally, indirect effects on agro-ecosystems include consideration of tritrophic feeding and broader system-level effects through targeted monitoring studies. Thus, characterization of protein class, history of use, and spectrum of activity provides relevant background to understand the nature of nontarget testing that will prove most relevant to ecological safety determinations.

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