Availability of chemosensory receptors is down-regulated by habituation of larvae to a morphogenetic signal.

Abstract

Larvae of the gastropod mollusc Haliotis rufescens are induced to settle from the plankton and metamorphose in response to exogenous y-aminobutyric acid (GABA) and a number of GABA-mimetic compounds, including a GABA-mimetic inducer uniquely associated with the surfaces of the naturally recruiting algae. Previous evidence has shown that recognition of these inducers is mediated by specialized chemosensory receptors on the larval epithelium and that transduction of the morphogenetic signal then is mediated by cAMP and excitatory depolarization. We demonstrate here the specific and saturable labeling of a population of larval receptors with the GABA analog f-(p-chlorophenyl)-[3H]GABA ([3H]baclofen); identification of these labeled receptors with those controlling metamorphosis is suggested by four independent criteria: (i) the effectiveness of GABA and its close structural analogs to induce metamorphosis is closely correlated with the effectiveness ofthese compounds to compete for binding to this receptor; (ii) the natural inducer purified from the recruiting algae competes for binding to this receptor; (iii) (-)-[3H]baclofen specifically bound to the receptors is shed from the larvae after %20 hr, at the time corresponding to the metamorphic abscission and shedding of sensory cilia and other structures from the larvae; and (iv) the availability of the receptors for labeling and the ability of the larvae to respond to GABA and GABA analogs can be down-regulated in parallel by habituation of the larvae early in their development. These down-regulated larvae are fully capable of settlement and metamorphosis in response to agents that elevate intracellular cAMP or depolarize the chemosensory membrane, confirming that down-regulation is confined to the receptors, with no effect on the postreceptor pathway. The results reported here thus suggest that the sensitivity of marine invertebrate larvae to morphogenetic stimuli from the environment can be downregulated by reduction in the number of chemosensory receptors available for interaction with the molecules that induce settlement and metamorphosis. In this respect, chemosensory receptors for environmental and morphogenetic signals are demonstrated biochemically to respond to habituation in a similar manner to neuronal and hormonal receptors.Larvae of many benthic marine invertebrate animals, after dispersal in the plankton, are induced to settle and metamorphose only upon recognition of specific substrata (1-8). Larvae (0.2 mm) of the Pacific red abalone, Haliotis rufescens, a gastropod mollusc, are induced to settle, attach to substrata, and metamorphose by chemosensory recognition of y-aminobutyric acid (GABA)-mimetic molecules that are uniquely associated with the surfaces of crustose red algae (9, 10). These purified natural inducers alone, GABA, and a number of GABA analogs are sufficient to induce this genetically programed behavioral and morphogenetic sequence (11-14); in the absence of such inducers, the larvae do not settle or metamorphose (11)(12)(13)...

Serotonin Injections Induce Metamorphosis in Larvae of the Gastropod Mollusc Ilyanassa obsoleta

“…It induces metamorphosis in Haliotis by mimicking the actions of the natural inducer at external chemoreceptors (Trapido-Rosenthal and Morse, 1985Morse, , 1986aBarlow, 1990;Wodicka and Morse, 1991). Injection of GABA provided a negative control for our study.…”

G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae

“…rufescens (red abalone) larvae were produced and reared as described (1,2,4,7). Assays were performed in duplicate at 15'C in glass vials containing =200 fully competent larvae (9 days old) in a final vol of 10 ml of fresh 5-,um-filtered ultraviolet-sterilized seawater, with rifampicin at 2 pkg/ml, and other compounds at the indicated concentrations.…”

“…The settlement and metamorphosis of Haliotis larvae in response to low concentrations of any of these inducers can be facilitated, or amplified, by several diamino acids structurally related to lysine, including L-a,3-diaminopropionic acid (DAPA) (see Fig. 1A), without altering the number or affinity of the GABA chemoreceptors (6)(7)(8).Recent evidence has shown that this facilitation of the morphogenetic response occurs at a postreceptor level independent of inducer binding at the GABA chemoreceptors (6). We present evidence here that transduction of the facilitating DAPA signal is mediated by a regulatory pathway that is separate from the morphogenetic pathway.…”

Settlement of benthic marine invertebrates

“…These authors have observed that a decrease in external potassium concentration inhibits induction by GABA, which could be due to hyperpolarization and which would antagonize the depolarization mediated by GABA. The activation of anionic channels would depend on enzymes phosphorylated by protein kinases A, which would, In turn, be activated by cAMP (Morse et al 1980, Trapido-Rosenthal & Morse 1986b. The levels of the latter would be increased by the activation of the adenylate cyclase through the binding of the exoyenoils liya~~ci jillductllj iu tile recepior jMorse i93i).…”