SYNOPSIS. The Cactus-Microorganism-Drosophila Model System of the Sonoran Desert represents an excellent paradigm of the role of chemistry in plant-animal interactions. In this system, four species of endemic Drosophila feed and reproduce in necrotic tissue of five species of columnar cacti. Studies over the past 35 yr have characterized a myriad of interactions between the three major components of the model system. The cacti contain a variety of allelochemicals which are primarily responsible for the highly specific pattern of host plant utilization exhibited by the desert Drosophila. Plant chemistry, through its effect on the microbially produced volatile patterns, is further involved in host specificity because the flies use the volatile pattern to cue in on necroses in the appropriate species of cactus. The metabolic activities of microorganisms (bacteria and yeasts) living in the necrosis can affect the substrate chemistry in both positive and negative ways (i.e., acting to increase or to decrease the toxicity of the substrate). Finally, cactus chemistry may affect drosophilid mating behavior since larval rearing substrate has been shown to influence adult hydrocarbon epicuticular composition. In D. mojavensis, adult hydrocarbon profile has been implicated as a determinant of mate choice leading to premating isolation between geographically isolated populations that use chemically different cactus substrates. Current research is focused on the evolution and regulation of genes whose products (cytochrome P450 enzymes) are involved in the specific insect-host plant relationships which exist between the Drosophila species and the cactus species.There are many reasons why investigators choose to focus their research efforts on what are referred to as ''model systems.'' Typically included among these would be the idea that model systems are easier to study because they are less complex than other scientific situations. At the same time, model systems should be representative of more complex, natural systems so that information that is obtained from their study is broadly applicable. For almost a century, the fruit fly, Drosophila melanogaster, has served as a model organism for the study of genetics. As a genetic paradigm, Drosophila is more tractable to scientific investigation than most organisms and has provided important insights into a wide variety of human maladies from alcohol abuse to neurological brain disorders (Bellen, 1998). Similarly, the interrelationships of the columnar cacti and the cactophilic Drosophila species of the Sonoran Desert have, for the past 35 yr, provided an excellent model system with which to study relevant questions in evolution, ecological genetics, and chemical ecology. The intent of this article is to briefly review and characterize the chemical interactions between the plants (cacti) and animals (Drosophila) of this model system, and, in addition, provide some thoughts on possible future directions for integrative approaches in this research area.

The mutualistic interactions of cactophilicDrosophila and their associated yeasts in the Sonoran Desert are studied as a system which has evolved within the framework of their host cactus stem chemistry. Because theDrosophila-yeast system is saphrophytic, their responses are not thought to directly influence the evolution of the host. Host cactus stem chemistry appears to play an important role in determining where cactophilicDrosophila breed and feed. Several chemicals have been identified as being important. These include sterols and alkaloids of senita as well as fatty acids and sterol diols of agria and organpipe cactus. Cactus chemistry appears to have a limited role in directly determining the distribution of cactus-specific yeasts. Those effects which are known are due to unusual lipids of organpipe cactus and triterpene glycosides of agria and organpipe cactus.Drosophilayeast interactions are viewed as mutualistic and can take the form of (1) benefits to theDrosophila by either direct nutritional gains or by detoxification of harmful chemicals produced during decay of the host stem tissue and (2) benefits to the yeast in the form of increased likelihood of transmission to new habitats. Experiments on yeast-yeast interactions in decaying agria cactus provide evidence that the yeast community is coadapted. This coadaptation among yeasts occurs in two manners: (1) mutualistic increases in growth rates (which are independent of the presence ofDrosophila larvae) and (2) stabilizing competitive interactions when growth reaches carrying capacity. This latter form is dependent on larval activity and results in benefits to the larvae present. In this sense, the coadapted yeast community is probably also coadapted with respect to itsDrosophila vector.

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Cytochrome P450s constitute a superfamily of genes encoding mostly microsomal hemoproteins that play a dominant role in the metabolism of a wide variety of both endogenous and foreign compounds. In insects, xenobiotic metabolism (i.e., metabolism of insecticides and toxic natural plant compounds) is known to involve members of the CYP6 family of cytochrome P450s. Use of a 3 RACE (rapid amplification of cDNA ends) strategy with a degenerate primer based on the conserved cytochrome P450 heme-binding decapeptide loop resulted in the amplification of four cDNA sequences representing another family of cytochrome P450 genes (CYP28) from two species of isoquinoline alkaloidresistant Drosophila and the cosmopolitan species Drosophila hydei. The CYP28 family forms a monophyletic clade with strong regional homologies to the vertebrate CYP3 family and the insect CYP6 family (both of which are involved in xenobiotic metabolism) and to the insect CYP9 family (of unknown function). Induction of mRNA levels for three of the CYP28 cytochrome P450s by toxic host-plant allelochemicals (up to 11.5-fold) and phenobarbital (up to 49-fold) corroborates previous in vitro metabolism studies and suggests a potentially important role for the CYP28 family in determining patterns of insect-host-plant relationships through xenobiotic detoxification.

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The yeast flora found in the major substrates of Drosophila mojavensis and in larval guts was studied both qualitatively and quantitatively. Quantitative studies show that, in four of the five substrates tested, the larvae did not contain a random sample of the yeasts present in the substrates. One widely distributed cactus yeast, Pichia cactophila, was typically in greater frequency in the larvae than in the substrates. Another cactus yeast, Candida sonorensis, typically exhibited the opposite relationship. Laboratory tests support larval preference behavior rather than differential digestion as being primarily responsible. Larvae are capable of distinguishing between patches of different yeast species and spend more time in patches of preferred yeasts. D. mojavensis appear to be ecological (host plants) generalists and physiological (yeasts) specialists in contrast to the other cactophilic Drosophila Selective feeding by D. mojavensis larvae in natural substrates may represent optimal foraging behavior.Interest in the microorganisms upon which Drosophila feed in nature dates back about 35 years (1-12). The researchers who participated in these early studies realized the importance of putting the population genetics ofDrosophila into an ecological context. Food sources are certainly major factors of the ecology of any animal, and yeasts are considered to be a major food source for the majority of species of Drosophila in both adult and larval stages (13). The last decade, however, has seen an acceleration ofinterest in this subject, particularly in the yeasts that inhabit the decaying stems of various species of columnar cacti in the Sonoran Desert.The Sonoran Desert of the southwestern United States and northwestern Mexico has provided a unique opportunity to study yeasts and their relationship to Drosophila species because the breeding and feeding sites of cactophilic Drosophila are well known (14,15 (26).The isolation ofyeasts from larval guts and specific substrates was accomplished as follows: Naturally occurring necroses were examined for the presence of Drosophila larvae. If they were present, three or four 1-g samples of the rotting tissue were collected from the area of the rot containing the larvae. Six to eight second-or third-instar larvae were also collected. The larvae were surface sterilized in 70% (vol/vol) The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact.

A total of 108 pectolytic, soft-rotting Erwinia strains were collected from 11 types of cacti growing in Arizona, Texas, northern Mexico, and Australia between 1958 and. Four strains were collected from soils beneath or close to naturally rotting saguaro cacti. Collectively, these strains caused soft rots of saguaro, organ pipe, and senita cacti, Opuntia (cactus) fruits and pads, tomato fruits, and potato slices, but only occasionally caused soft rots of slices of carrot roots. A numerical cluster analysis showed that 98 of the 112 strains formed a uniform group (cluster 1A) that was distinguished from other pectolytic erwinias by an API 20E code of 1205131, by negative reactions in API 5OCHE tests for L-arabinose, myo-inositol, D-cellobiose, melibiose, and D-raffinose, and, in supplemental tests, by positive reactions for malonate and growth at 43°C. The average levels of DNA relatedness of 22 cluster 1A strains to the proposed type strain (strain 1-12) as determined by the hydroxyapatite method were 88% in 60°C reactions (with 1% divergence within related sequences) and 87% in 75°C reactions. The levels of relatedness to the type strains of other Erwinia spp. were 138% in 75°C reactions. Cluster 1A strains also had a characteristic cellular fatty acid profile containing cyclo-( 11,12)-nonadecanoic acid (C19:o cycle cll-lz) and missing tridecanoic acid (CI3J, heptadecanoic acid (C1,:o), and cis-9-heptadecenoic acid (Cl,:l g ) , which separated them from other pectolytic erwinias. Collectively, these data indicate that the members of cluster 1A are members of a new species, which we name Erwinia cacticida. Three cactus strains in cluster 1B appear to represent a second new species that is closely related to E. cacticida; these strains are designated E . cacticida-like pending the availability of additional strains for testing. The remaining cactus strains (in cluster 4) have the physiological, DNA, and fatty acid profiles of Erwinia carotovora.To our knowledge, Johnston and Hitchcock (22) were the first workers to describe a bacterial soft-rot disease of cacti in the United States. The cultures of these authors were isolated from prickly pear cacti (Opuntia tomentella Berger and OpuntiaJicus-indica (L.) Mill.) that were originally from Guatemala and Columbia but were growing in the U.S. Department of Agriculture plant introduction garden in Florida. The bacterium was briefly characterized as "an actively motile, gram-negative, aerobic, and facultative anaerobic bacillus" which produced an acid reaction when it was grown in broth containing "glucose, saccharose, mannite, and salicin but none in maltose, lactose, dulcite, and arabinose" (22). Subsequently, another new bacterial species, Erwinia carnegieana Standring 1942 (23), was described (3, 6, 23, 28) as being the causal agent of bacterial necrosis (a soft-rot disease) of saguaro cacti (Carnegiea gigantea Britt. & Rose). Among the soft-rot erwinias, this species was unique in that it was gram positive, a characteristic also noted by Boyle (6), and had a host ...