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Postgenomic Chemical Ecology: from Genetic Code to Ecological Interactions1

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Postgenomic Chemical Ecology: from Genetic Code to Ecological Interactions1 P1: GVM Journal of Chemical Ecology [joec] pp452-joec-370876 April 20, 2002 11:25 Style file version Nov. 19th, 1999 Journal of Chemical Ecology, Vol. 28, No. 5, May 2002 (C 2002) POSTGENOMIC CHEMICAL ECOLOGY: FROM GENETIC CODE TO ECOLOGICAL INTERACTIONS1 MAY R. BERENBAUM2, 2Department of Entomology, 320 Morrill Hall University of Illinois 505 S. Goodwin Urbana, Illinois 61801-3795 (Received June 26, 2001; accepted January 12, 2002) Abstract—Environmental response genes are defined as those encoding pro- teins involved in interactions external to the organism, including interactions among organisms and between the organism and its abiotic environment. The general characteristics of environmental response genes include high diver- sity, proliferation by duplication events, rapid rates of evolution, and tissue- or temporal-specific expression. Thus, environmental response genes include those that encode proteins involved in the manufacture, binding, transport, and breakdown of semiochemicals. Postgenomic elucidation of the function of such genes requires an understanding of the chemical ecology of the organism and, in particular, of the “small molecules” that act as selective agents either by pro- moting survival or causing selective mortality. In this overview, the significance of several groups of environmental response genes is examined in the context of chemical ecology. Cytochrome P-450 monooxygenases provide a case in point; these enzymes are involved in the biosynthesis of furanocoumarins (furo- coumarins), toxic allelochemicals, in plants, as well as in their detoxification by lepidopterans. Biochemical innovations in insects and plants have historically been broadly defined in a coevolutionary context. Considerable insight can be gained by defining with greater precision components of those broad traits that contribute to diversification. Molecular approaches now allow chemical ecol- ogists to characterize specifically those biochemical innovations postulated to lead to adaptation and diversification in plant/insect interactions. Key Words—Allelochemical, cytochrome P-450, environmental response gene, Helicoverpa, olfactory receptor, Papilio, substrate recognition site, xenobiotic response element, furanocoumarin, furocoumarin. 1 ISCE-Silverstein/Simeone Award 2000. E-mail: [email protected] 873 0098-0331/02/0500-0873/0 C 2002 Plenum Publishing Corporation P1: GVM Journal of Chemical Ecology [joec] pp452-joec-370876 April 20, 2002 11:25 Style file version Nov. 19th, 1999 874 BERENBAUM INTRODUCTION The millenium bug, or Y2K bug, is the computer glitch that was a function of the fact that, in the 1950s, IBM engineers, to save memory, used only a two- digit year field; the two-digit field was anticipated to wreak havoc after December 31, 1999 (Anonymous, 2000). Such havoc conspicuously failed to materialize. Thus, an insect perhaps more worthy of the designation Y2K bug is Drosophila melanogaster, the vinegar or pomace fly. In March 2000, sequencing of the en- tire genome of D. melanogaster was completed and published, marking the first complete arthropod genome to be sequenced (Adams et al., 2000). This accom- plishment may herald a new era within the field of chemical ecology. Since its inception, practitioners of the science of chemical ecology have been concerned mostly with small molecules. Admittedly, some reach impressive size; a case in point may be the extremely large-ring monocyclic polyazamacrolides produced in the defensive secretions of some coccinellid pupae. Ring sizes in some of these remarkable macrocycles can range from 24 to over 150 members (Schroeder et al., 2000), but substances with the cognomen “macromolecules” are only recently subjects for study by chemical ecologists. Protein serving as olfactory receptors and enzymes involved in allelochemical biosynthesis now routinely merit study, but even bigger molecules loom on the horizon. In the postgenome era, DNA should be an increasing focus of attention even for those with an affection for small, tractable molecules. One reason is that DNA itself is a target site for many toxic natural products. The universal occurrence of DNA makes it a likely evolutionary target for broad-spectrum defense com- pounds, and the evolution of DNA must reflect in part interspecific interactions among organisms. B-DNA possesses quite a number of nucleophilic reactive sites that interact with natural products (Yangand Wang, 1999). Furanocoumarins (furo- coumarins), e.g., benz-2-pyrone compounds produced by a handful of angiosperm plants primarily in the Apiaceae and Rutaceae, covalently bind to thymine and cross-link strands. Ecteinascidin from the marine tunicate Ecteinascidia turbinata binds covalently to guanine N-2; the fungal metabolite aflatoxin B1 attacks N-7 guanine. Duacarmycin, a Streptomyces product, and bleomycin/pepleomycin, from Streptomyces verticillus, induce DNA backbone cleavage. Daunorubicin, initially isolated from Streptomyces caeruleorubidus, and doxorubicin, produced by Strep- tomyces peucetius, are anthracycline drugs that can intercalate (as can triostin A and echinomycin, naturally occurring bisintercalator quinoxaline antibiotics from Streptomyces echinatus and related species); distamycin A, from Streptomyces distallicus, binds in the narrow minor groove associated with AT sequences in B-DNA, and actinomycin D from Streptomyces spp. binds to DNA duplexes and interferes with transcription. Perhaps a more important reason for chemical ecologists to incorporate DNA into their studies is that one of the principal goals of postgenomic biology is to P1: GVM Journal of Chemical Ecology [joec] pp452-joec-370876 April 20, 2002 11:25 Style file version Nov. 19th, 1999 POSTGENOMIC CHEMICAL ECOLOGY 875 ascertain gene function, and the function of many genes can be comprehended only within the context of chemical ecology, in particular, the function of those genes that can be considered “environmental response genes.” Environmental response genes can be defined as those encoding proteins involved in interactions external to the organism, including interactions among organisms and between the organ- ism and its abiotic environment. General characteristics of environmental response genes, particularly those involved in mediating interactions among organisms and thus allowing for reciprocal evolutionary responses, include (1) very high diversity, (2) proliferation by duplication events, (3) rapid rates of evolution, (4) occurrence in gene clusters, and (5) tissue- or temporal-specific expression. All of these char- acteristics are consistent with responses to evolutionary pressure emanating from a highly changeable external environment. Among environmental response genes, then, are those encoding proteins in- volved in the manufacture, binding, transport, and breakdown of semiochemicals, the principal medium of communication for many species between the organism and its environment. Examples of environmental response genes are numerous. Chemical signals are characterized by producers and recipients, and each has its own set of genes (Table 1). These genes may have genome-level effects that are very different from, for example, the so-called “housekeeping genes.” By the same token, the term in common use to contrast with housekeeping genes, i.e., “luxury genes” (e.g., Vinogradov, 1997), sells short the ecological and evolutionary contri- butions of genes allowing organisms to cope with environmental stress. The lack of correlation between genome size and number of genes (e.g., Caenorhabditis elegans at 97 Mb and 19,000 genes and Drosophila melanogaster with 180 Mb and 13,000 genes; http://www.ornl.gov/hgmis/faq/compgen.html) has led to the suggestion that evolution proceeds principally by altering patterns of gene ex- pression, rather than by increasing the protein inventory. Environmental response genes may be an exception to the trend; new functions may be acquired by prolif- eration of new proteins, not just by changes in regulation and expression. Parallel evolution in both gene function and expression pattern may be the key to diver- sification in environmental response genes. In this overview, the significance of TABLE 1. SEMIOCHEMICALS AND ASSOCIATED ENVIRONMENTAL RESPONSE GENES Semiochemical Producer Receiver Pheromone Biosynthetic genes Pheromone-binding protein genes Odorant receptor genes Pheromone-degrading enzymes Allomone Biosynthetic genes Detoxification genes Transport protein genes Transport protein genes Kairomones Biosynthetic genes Odorant receptor genes Taste receptor genes P1: GVM Journal of Chemical Ecology [joec] pp452-joec-370876 April 20, 2002 11:25 Style file version Nov. 19th, 1999 876 BERENBAUM several groups of environmental response genes is examined in the context of chemical ecology. The “chemical senses” by which organisms perceive information about their environments encompass olfaction, or perception of chemical stimuli in gaseous phase, and gustation (and other forms of contact chemoreception), perception of chemical stimuli as solutes in liquid media. Irrespective of organism, chemical signaling (not only externally but also internally) shares several features. Most, if not all, chemical signaling systems include a receptor that reacts with a signal molecule; many also involve a signal transducer and amplifier. Perireceptor phe- nomena associated with movement of signal molecules (binding, transport, and degradation) also share many conserved features across a wide range of taxa. Many of the same classes of molecules serve these functions across
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