Abstract
Detoxification enzymes play a key role in plant-herbivore interactions, contributing to the on-going evolution of ecosystem functional diversity. Mammalian detoxification systems have been well studied by the medical and pharmacological industries to understand human drug metabolism; however, little is known of the mechanisms employed by wild herbivores to metabolize toxic plant secondary compounds. Using a wild rodent herbivore, the desert woodrat (Neotoma lepida), we investigated genomic structural variation, sequence variability, and expression patterns in a multigene subfamily involved in xenobiotic metabolism, cytochrome P450 2B (CYP2B). We hypothesized that differences in CYP2B expression and sequence diversity could explain differential abilities of woodrat populations to consume native plant toxins. Woodrats from two distinct populations were fed diets supplemented with either juniper (Juniperus osteosperma) or creosote bush (Larrea tridentata), plants consumed by woodrats in their respective desert habitats. We used Southern blot and quantitative PCR to determine that the genomic copy number of CYP2B in both populations was equivalent, and similar in number to known rodent copy number. We compared CYP2B expression patterns and sequence diversity using cloned hepatic CYP2B cDNA. The resulting sequences were very diverse, and clustered into four major clades by amino acid similarity. Sequences from the experimental treatments were distributed non-randomly across a CYP2B tree, indicating unique expression patterns from woodrats on different diets and from different habitats. Furthermore, within each major CYP2B clade, sequences shared a unique combination of amino acid residues at 13 sites throughout the protein known to be important for CYP2B enzyme function, implying differences in the function of each major CYP2B variant. This work is the most comprehensive investigation of the genetic diversity of a detoxification enzyme subfamily in a wild mammalian herbivore, and contributes an initial genetic framework to our understanding of how a wild herbivore responds to critical changes in its diet.
Highlights
The interactions between plants and their herbivores represent a large and important fraction of the relationships in any ecosystem
We explored the potential for genetic diversity in the cytochrome P450 2B (CYP2B) subfamily to explain how Mojave Desert woodrats are able to ingest greater quantities of creosote resin than Great Basin woodrats
Woodrat CYP2B characterization The cDNA resulting from the CYP2B sequencing effort was 1476 bp from start to stop codons (Figure S1)
Summary
The interactions between plants and their herbivores represent a large and important fraction of the relationships in any ecosystem. A number of enzymes in the liver metabolize plant secondary compounds (PSCs) and other xenobiotics by modifying them to more excretable compounds by increasing the polarity through the addition of functional groups or endogenous conjugates. These hepatic biotransformation (‘‘detoxification’’) enzymes are promiscuous; they perform a specific chemical function, they are not specific to a single substrate and react with many dietary toxins [2,3]. It is likely that the diversity, capacity and functionality of the liver biotransformation system evolved, in part, as adaptive strategy to cope with the large variety of PSCs encountered in nature [4]
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