Developmental and Morphogenetic Gene Regulation inHaliotis rufescensLarvae at Metamorphosis

Abstract

The planktonic larva of the red abalone, Haliotis rufescens, must develop competence and recognize an appropriate exogenous morphogenetic cue before it can settle and metamorphose. The molecular mechanisms underlying the development of larval competence and the induction of metamorphosis in this and other marine invertebrates are only now starting to be understood. In Haliotis, some of the morphogenetic cues, chemosensory receptors, and receptor-mediated signal transduction pathways controlling the induction of metamorphosis from the planktonic larva to the benthic post-larva have been identified. To ascertain how these initial signaling pathways regulate the global changes that occur at metamorphosis, we have investigated the expression of two classes of genes: (i) those that are expressed but not thought to be functionally required in the veliger larva, and (ii) those that exhibit marked changes in tissue-specific expression induced at metamorphosis. Expression of the genes encoding a larval chymotrypsin and a muscle-specific tropomyosin reveal two distinct developmental pathways governing gene expression and metamorphosis in Haliotis; changes in the synthesis of other proteins and in morphology support this conclusion. One of these pathways, termed the morphogenetic pathway, is linked directly to the processes of settlement and metamorphosis; the induction of tropomyosin in the adult columellar muscle progenitors 48 hr after induction of metamorphosis provides the best and most direct evidence at the molecular level for the existence of this pathway in Haliotis. The other pathway, which we have termed the anticipatory (or preparatory) pathway, is first activated prior to or at the attainment of larval competence, and is induced again at metamorphosis. The induction of expression of a chymotrypsin gene in migrating digestive amoebocytes in the larva, and the depletion of tropomyosin mRNA from cells of the larval retractor muscle, provide molecular evidence for this program. We review here the patterns of expression of these genes, and suggest that the uncoupling of these pathways reflects an adaptation of Haliotis larval development to meet the future demands of benthic life.