Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera

Abstract

A great diversity of pheromone structures are used by moth species (Insecta: Lepidoptera) for long-distance mating signals. The signal͞ response channel seems to be narrow for each species, and a major conundrum is how signal divergence has occurred in the face of strong selection pressures against small changes in the signal. Observations of various closely related and morphologically similar species that use pheromone components biosynthesized by different enzymes and biosynthetic routes underscore the question as to how major jumps in the biosynthetic routes could have evolved with a mate recognition system that is based on responses to a specific blend of chemicals. Research on the desaturases used in the pheromone biosynthetic pathway for various moth species has revealed that one way to make a major shift in the pheromone blend is by activation of a different desaturase from mRNA that already exists in the pheromone gland. Data will be presented to support the hypothesis that this process was used in the evolution of the Asian corn borer, Ostrinia furnacalis species. In that context, moth sex-pheromone desaturase genes seem to be evolving under a birth-and-death process. According to this model of multigene family evolution, some genes are maintained in the genome for long periods of time, whereas others become deleted or lose their functionality, and new genes are created through gene duplication. This mode of evolution seems to play a role in moth speciation, as exemplified by the case of the Asian corn borer and European corn borer, Ostrinia nubilalis species.C hemical communication systems in insects have provided exciting challenges to researchers in chemistry, biochemistry, physiology, ecology, genetics, and behavior for over four decades. Much of this research has been focused on moths in the order Lepidoptera, which is the second largest insect order with well over a hundred thousand described species. Most of the hundreds of species studied have been found to use a long-distance chemical communication system for attracting mates (www.nysaes. cornell.edu͞fst͞faculty͞acree͞pheronet͞index.html). Initially, pheromone components were characterized, and behavior mediated by these chemical cues was studied. However, increased knowledge of the precise blends used by different species only raised more questions on many aspects of the communication system. Underlying these questions was the fundamental curiosity about the extensive radiation seen in moths and what role pheromones played in the speciation process. How did sex pheromones evolve and could changes in this mating system give rise to isolated populations that become new species? Studies on pheromone biosynthetic pathways provided basic information on this issue, but the use of molecular techniques in the postgenomics era has become essential in addressing these questions. Pheromone Biosynthetic PathwaysBy the 1980s, many moth pheromone components had been characterized, and a majority were acetates, alcohols, or aldehydes with long hydrocarbon ch...

Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori , sex pheromone

“…This selective partitioning is undoubtedly the result of the enzyme's bifunctionality and clearly demonstrates the divergence of the B. mori Desat1 from the other ⌬11 desaturases. Analysis of the other pheromone gland-derived desaturases indicates that desat4 can be clustered with ⌬9 desaturases, whereas desat5 can be grouped within the ⌬10,11 branch of desaturase genes (20).…”

“…For other desaturase genes expressed in the pheromone gland, poly(A) ϩ RNA (300 ng) was prepared with the MICROFAST-TRACK 2.0 mRNA isolation kit (Invitrogen) and reversetranscribed with Oligo(dT) 20 by using the Thermoscript RT-PCR system (Invitrogen). To amplify DNA fragments of all of the desaturase genes present, a set of degenerate primers, DsF (5Ј-AT H ACNGCNGGNGCNCAYMG-3Ј) and DsR (5Ј-AANRYRTGRTGRTARTTRTG-3Ј), were designed from the conserved sequences encoding the first and third histidinecluster regions of known insect desaturases (4).…”

Cloning and Characterization of the Pheromone Biosynthesis Activating Neuropeptide Receptor from the Silkmoth, Bombyx mori

“…moths and butterflies), the successful propagation of individual species is dependent on the female's ability to attract conspecific males; an event mediated by species-specific blends of volatile compounds known as sex pheromones (1). These sex pheromones are produced and released by a specialized gland, appropriately known as the pheromone gland (PG), 1 located between the eighth and ninth abdominal segments of the female. A major class of pheromone components produced by female moths is the C 10 -C 18 unsaturated, acyclic, aliphatic compounds that contain an oxygenated functional group such as aldehyde, alcohol, or acetate ester.…”

Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion

“…Biosynthesis of these blends involves three key enzymatic components: uncharacterized enzymes that mediate limited chainshortening reactions, reductases that convert acyl intermediates into alcohols, and sex pheromone desaturases that introduce double bonds at specific locations along the hydrocarbon chain. Moth sex pheromone desaturases are part of a larger family of insect acyl-CoA desaturases that originated several hundred Mya (1). So far, five distinct desaturase subfamilies have been discovered and found to function in the biosynthesis of female moth sex pheromone blends (2).…”

“…Because sex pheromone desaturases are key players in moth reproduction, an understanding of the mechanisms that are responsible for generating their diversity may shed light on the molecular processes that underlie speciation in this group of insects. Thus, we initiated research to examine the diversity of sex pheromone desaturase genes and their patterns of evolution in the genomes of the ECB and ACB, two representative moth species for which a considerable amount of knowledge concerning their pheromone blends and chemical communication systems has been amassed over the past few decades (1,(4)(5)(6)(7)(8)(9). Surprisingly, we found that an even larger number of ''cryptic'' sex pheromone desaturase genes exist within corn borer genomes and that these novel genes were generated as a result of a fusion event with a retroposon.…”