G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae

Abstract

The regulatory guanine nucleotide binding protein (G protein) activators cholera toxin and the GTP analog 5-guanylyl imidophosphate, the second messenger diacylglycerol, and certain diamino acids all facilitate (amplify) the settlement and metamorphic responses of planktonic larvae of Haliotis rufescens (marine mollusc) to morphogenetic chemical stimuli. In contrast, the G protein-inhibiting analog guanosine 5'-0-[,B-thioldiphosphate inhibits facilitation by L-a,4-diaminopropionic acid but does not block facilitation by diacylglycerol. Diacylglycerol, cholera toxin, and the guanine nucleotide analogs alone neither induce the settlement and metamorphosis of the larvae nor do they inhibit induction of metamorphosis by y-ammnobutyric acid. These results thus establish the existence of separate regulatory and inductive pathways controlling larval metamorphosis in response to two classes of exogenous chemical signals from the environment. The regulatory pathway, operating independently through a G protein-diacylglycerol cascade apparently controlled by facilitating diamino acids in the water column, can amplify the larval responsiveness to inducers of metamorphosis. This mechanism may have adaptive significance in the recognition and selection of favorable habitats for metamorphosis of the larvae. Similar regulatory pathways, based on exogenous control of a G protein-diacylglycerol cascade, may govern responsiveness to stimuli in other sensory and developmental systems.Planktonic larvae of the marine gastropod mollusc Haliotis rufescens are induced to settle from the water column, attach to substrate, and metamorphose in response to exogenous y-aminobutyric acid (GABA)-mimetic peptides that are found at the surfaces of specific algae; GABA and GABA analogs also induce this metamorphosis (1-5). The morphogenetic peptides, GABA, and GABA analogs all are recognized by a discrete population of larval chemosensory receptors that have been characterized directly by radioligand binding (5-7). 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. Our evidence suggests that this regulatory pathway involves a diacylglycerol second messenger and that the level of this second messenger is regulated by a guanine nucleotide binding protein. MATERIALS AND METHODS, and rifampicin were purchased from Sigma. DAPA was from CalbiochemBehring. The cyanobacterial GABA-mimetic peptide fraction was obtained as described (9). P...

Influence of delayed metamorphosis on postsettlement survival and growth in the sipunculan Apionsoma misakianum

“…Excess K' has subsequently been found to stimulate metamorphosis in a number of other species, including other gastropods, bryozoans, echinoids, sponges, hydrozoans, and polychaetes (Avila 1998;Boettcher & Targett 1998;Diggers & Laufer 1999; older literature reviewed by Pearce & Scheibling 1994;Woollacott & Hadfield 1996). Its widespread effectiveness suggested that excess K stimulates metamorphosis by depolarizing external receptor cells (Baloun & Morse 1984;Yool et al 1986;Baxter & Morse 1987;Chevolot et al 1991;Ilan et al 1993). If that is a singular and universal effect, we would expect all competent marine invertebrate larvae to metamorphose in response to excess K + , regardless of what chemical cues trigger metamorphosis naturally (Yool et al 1986).…”

Nitric Oxide Acts as a Positive Regulator to Induce Metamorphosis of the Ascidian Herdmania momus

“…The binding of environmental cues to cell surface receptors on the larval sensory organs transmits signals via the larval nervous system to activate biochemical signalling pathways that drive the global morphogenetic events of metamorphosis [12], [13]. Not surprisingly then, settlement and metamorphosis of many species can successfully be induced in vitro , by the application of synthetic chemical agents that activate or inhibit parts of these signalling pathways that are conserved among metazoans [14]–[18].…”

An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

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