Effect of allatectomy and ventral nerve cord transection on calling, pheromone emission and pheromone production in Lymantria dispar

Isolated abdomen and pheromone gland bioassays were utilized to determine the physiological action of the pheromone-biosynthesis-activating neuropeptide (PBAN) in the corn earworm moth Helicoverpa (= Heliothis) zea. An isolated pheromone gland bioassay showed that synthetic PBAN was active at 0.02 pmol, with maximal activity occurring at 0.5 pmol and 60 min of incubation. Second-messenger studies demonstrated that extracellular Ca2+ is necessary for PBAN activity on isolated pheromone glands. The Ca2+ ionophore A23187 stimulated pheromone biosynthesis alone, whereas the Ca2+ channel blockers La3' and Mn2+ inhibited PBAN activity. However, the organic Ca2+ channel blockers verapamil and nifedipine did not inhibit PBAN activity. Both forskolin and two cAMP analogues stimulated pheromone biosynthesis in the absence of extracellular Ca2+, indicating that Ca2+ may activate an adenylate cyclase. The biogenic amine octopamine did not elicit pheromone production in isolated gland or abdomen bioassays or when in ected into intact female moths. Removal of the ventral nerve chord, including the terminal abdominal ganglia in isolated abdomens, did not affect PBAN stimulation of pheromone production. Similar levels of stimulation were found when isolated abdomens were treated with PBAN in scotophase or photophase.Sex pheromone titers in most moths, including the corn earworm moth Helicoverpa (= Heliothis) zea, fluctuate diurnally with little or no pheromone present during the day and with peak pheromone titers occurring during midscotophase (1). This fluctuation is caused by the release and/or degradation of existing pheromone and the biosynthesis of new pheromone at precise times of the photoperiod. The biosynthesis of pheromone in H. zea is regulated by a peptide produced in the subesophageal ganglion (SEG) portion of the brain complex of female moths (2). This peptide, termed pheromone-biosynthesis-activating neuropeptide (PBAN), has been isolated and sequenced from brains of H. zea (3).Two other pheromonotropic peptides, each with about 80%o sequence identity with H. zea PBAN, have been isolated from the brains of the silkworm, Bombyx mori (4, 5). These peptides have been synthesized and the synthetic peptides retain biological activity, with cross-reactivity occurring in other species of moths (3, 4, 6, 7). These reports and others indicate that a variety of moths utilize PBAN or PBAN-like peptides in controlling pheromone biosynthesis.Although PBAN or PBAN-like activity has been identified in several different moth species, the physiological mode of action of PBAN has not been determined conclusively for any one species. In fact, there are two apparently conflicting hypotheses on how PBAN activates pheromone biosynthesis, and both are based on studies utilizing Heliothis moths as experimental animals. One hypothesis suggests that PBAN is synthesized in the SEG, transported to the corpora cardiaca, and then released into the hemolymph, where it can act on the pheromone gland to induce pheromone biosynthesis (8)....

mentioning

confidence: 98%

Stimulation of pheromone biosynthesis in the moth Helicoverpa zea: action of a brain hormone on pheromone glands involves Ca2+ and cAMP as second messengers.

Jurenka

Jacquin

Roelofs

1991

“…These experiments suggest that PBAN stimulates one or more neurons in the TAG that provide a signal to the gland to produce pheromone and that this signal is blocked in the nerve transection experiments. Previous studies in the gypsy moth Lymantria dispar also had shown that pheromone production depends on an intact nervous system (21)(22)(23), but the neural mechanisms linking the nervous system to the PG remained unresolved.…”

mentioning

confidence: 99%

Innervation and neural regulation of the sex pheromone gland in female Heliothis moths.

Christensen

Itagaki

Teal

et al. 1991

Female Heliothis moths normally produce their species-specific male attractant (sex pheromone blend) during scotophase, and this production is stimulated by pheromone biosynthesis activating neuropeptide (PBAN), presumably carried in the hemolymph. Several lines of evidence indicate that the central nervous system plays another critical role in this regulation. Pheromone biosynthesis was induced during photophase by electrical stimulation of the ventral nerve cord or the peripheral nerves projecting from the terminal abdominal ganglion to the pheromone gland in the tip of the abdomen. Electron microscopy further revealed that axonal branches innervate the gland tissue. Nerve branches associated with pheromone gland cells are enwrapped in glia and contain dense-core vesicles, suggesting that the innervation of the gland might be neurosecretory. Finally, the biogenic monoamine octopamine was nearly as effective as purified Heliothis zea PBAN in stimulating pheromone biosynthesis when injected into intact females during mid-photophase. Furthermore, both octopamine and PBAN stimulated significant increases in the pheromone content of the glands in isolated abdomens lacking a ventral nerve cord but only when abdomens were treated at the onset of scotophase. These data suggest that the regulation of sex pheromone production in Heliothis is more complex than previously thought. Activation of the gland appears to be governed by both neural and hormonal mechanisms, and these control mechanisms depend on photoperiodic cues.

“…Although these processes are tightly coordinated, no single neural, neuroendocrine, or endocrine factor regulates the complete system. In fact, there are conflicting reports (6)(7)(8)(9)(10)(11) regarding the endogenous mechanisms that control even a single aspect of the pheromone communication system in moths: induction of pheromone biosynthesis.…”

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confidence: 99%

“…It was hypothesized that the neuropeptide responsible, pheromone biosynthesis activating neuropeptide (PBAN), was released from the corpora cardiaca, carried in the hemolymph, and acted directly on the cells of the pheromone gland (4,6). However, gypsy moths, which also produce PBAN (6), do not require either the corpora allata or corpora cardiaca for production and release of the sex pheromone but do require that the ventral nerve cord be intact for production and release of normal amounts of pheromone (9)(10)(11). Thus, in this case neural rather than hormonal factors appear to be the main components regulating biosynthesis.…”

mentioning

confidence: 99%

Neural regulation of sex pheromone biosynthesis in Heliothis moths

Teal

Tumlinson

Oberlander

1989

Pheromone biosynthesis in females of Heliothis zea is regulated endogenously by a neuropeptide produced in the subesophageal ganglion. We have found that the ventral nerve cord must be intact for normal induction of pheromone biosynthesis and that pheromonotropic activity is associated with extracts of the abdominal nerve cord, but only during the period when pheromone is produced. We did not find evidence of pheromonotropic activity in hemolymph obtained from females that were producing pheromone. Extracts of the brain-subesophageal ganglion complex, which contain pheromone biosynthesis activating neuropeptide (PBAN), induced pheromone biosynthesis when applied to the terminal abdominal ganglion only if nerves from this ganglion to the pheromone gland were intact. Brain-subesophageal ganglion extracts did not induce biosynthesis when applied directly to the pheromone glands in vitro. From our results, we conclude that the target site of PBAN is not the pheromone gland but the terminal abdominal ganglion, and we hypothesize that the abdominal nerve cord transports PBAN to the terminal abdominal ganglion.Endogenous regulation of reproductive physiology and behavior associated with pheromone production and release in many insects results from the action of nervous, neuroendocrine, and/or endocrine stimulation (1-4). However, while the chemistry and biological effects of sex pheromones are understood more fully for moth species than for other groups of insects (5), the endogenous mechanisms that regulate the initiation and inhibition of pheromone biosynthesis by moths remain largely unexplored. Neural, neurohormonal, and hormonal regulators effectively control the periodicity of sexual signaling and are thus of prime importance for the reproductive success of moth species. Although these processes are tightly coordinated, no single neural, neuroendocrine, or endocrine factor regulates the complete system. In fact, there are conflicting reports (6-11) regarding the endogenous mechanisms that control even a single aspect of the pheromone communication system in moths: induction of pheromone biosynthesis.Studies on the corn earworm moth Heliothis zea (6-8) have firmly established that injection of extracts of the subesophageal ganglion induces pheromone biosynthesis. It was hypothesized that the neuropeptide responsible, pheromone biosynthesis activating neuropeptide (PBAN), was released from the corpora cardiaca, carried in the hemolymph, and acted directly on the cells of the pheromone gland (4, 6). However, gypsy moths, which also produce PBAN (6), do not require either the corpora allata or corpora cardiaca for production and release of the sex pheromone but do require that the ventral nerve cord be intact for production and release of normal amounts of pheromone (9-11). Thus, in this case neural rather than hormonal factors appear to be the main components regulating biosynthesis.These apparent discrepancies in the regulation of pheromone production caused us to investigate the mechanism by which PBAN ind...