Delayed and asynchronous ganglionic maturation during cephalopod neurogenesis as evidenced by Sof‐elav1 expression in embryos of Sepia officinalis (Mollusca, Cephalopoda)

Abstract

Among the Lophotrochozoa, centralization of the nervous system reaches an exceptional level of complexity in cephalopods, where the typical molluscan ganglia become highly developed and fuse into hierarchized lobes. It is known that ganglionic primordia initially emerge early and simultaneously during cephalopod embryogenesis but no data exist on the process of neuron differentiation in this group. We searched for members of the elav/hu family in the cuttlefish Sepia officinalis, since they are one of the first genetic markers of postmitotic neural cells. Two paralogs were identified and the expression of the most neural-specific gene, Sof-elav1, was characterized during embryogenesis. Sof-elav1 is expressed in all ganglia at one time of development, which provides the first genetic map of neurogenesis in a cephalopod. Our results unexpectedly revealed that Sof-elav1 expression is not similar and not coordinated in all the prospective ganglia. Both palliovisceral ganglia show extensive Sof-elav1 expression soon after emergence, showing that most of their cells differentiate into neurons at an early stage. On the contrary, other ganglia, and especially both cerebral ganglia that contribute to the main parts of the brain learning centers, show a late extensive Sof-elav1 expression. These delayed expressions in ganglia suggest that most ganglionic cells retain their proliferative capacities and postpone differentiation. In other molluscs, where a larval nervous system predates the development of the definitive adult nervous system, cerebral ganglia are among the first to mature. Thus, such a difference may constitute a cue in understanding the peculiar brain evolution in cephalopods.

Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopods

“…Sof‐pax3/7 expression provided new insights into the differentiation of the epidermis, and the expression of Sof‐elav1 , a member of the elav/hu family and one of the first genetic markers of postmitotic neural cells in metazoans (Campos et al, ; Sakakibara et al, ; Buresi et al, ), permitted early labelling of developing neurons in S. officinalis . Expression patterns of Sof‐elav1 thus provided a new perspective of the early development of the peripheral nervous system, as they did previously for the developing central nervous system of this organism (Buresi et al, ). Here, Sof‐elav1 expression demonstrates that the two developing olfactory organs were the first ectodermal sensory structures in which differentiating neurons were detected, at about stage 16 (Fig.…”

“…The 687-bp fragment of Sof-elav1 was found to be orthologous to the neurogenic member of the elav/hu family (accession No. HE956712.1; see Buresi et al, 2013). The 783-bp fragment of Sof-pax3/7 (accession No.…”

“…In vertebrates, pax3 and pax7 code for transcription factors that intervene in the development of the neural crest cells, in particular, the progenitor cells of melanocytes and the future peripheral neurons (Le Douarin and Kalcheim, ). In addition, we examined the expression of the S. officinalis homolog of elav1 ( Sof‐elav1 ) in the embryo ectoderm, because this gene is one of the first markers of differentiating and differentiated neurons in most metazoans (Campos et al, ; Sakakibara et al, ; Denes et al, ; Marlow et al, ), including S. officinalis (Buresi et al, ). The differentiated sensory cells were finally described via confocal imaging in late embryos of S. officinalis and in hatchlings of other coleoid species for comparisons, in the nectobenthic species Euprymna scolopes (Sepiolidae) and in the pelagic species Doryteuthis opalescens (Teuthidae).…”

Eye development and photoreceptor differentiation in the cephalopod Doryteuthis pealeii

“…Moreover, adult neuroanatomy of multiple cephalopod species has been well described (Young, 1962a(Young, ,b, 1971Nixon and Young, 2003;Wild et al, 2015). Despite these elegant studies, gene expression is only now being explored during development, and detailed molecular and genomic analyses of cephalopod organogenesis are in their infancy Hartmann et al, 2003;Lee et al, 2003;Baratte et al, 2007;Farfán et al, 2009;Navet et al, 2009;Buresi et al, 2012Buresi et al, , 2013Buresi et al, , 2016Ogura et al, 2013;Focareta et al, 2014;Peyer et al, 2014;Wollesen et al, 2014;Yoshida et al, 2014;Shigeno et al, 2015;Wollesen et al, 2015). The cephalopod eye is a single-chambered eye generated from an internalization of the optic placode (Gilbert et al, 1990).…”

Reversion to developmental pathways underlies rapid arm regeneration in juvenile European cuttlefish, Sepia officinalis (Linnaeus 1758)

“…This study focused on three genes associated with early tissue speciation. Previous studies have identified many genes implicated in cephalopod limb morphogenesis; future experimentation would especially benefit from timepoint‐ and treatment‐specific profiles, with particular emphasis on genes associated with nervous precursor distribution and development of complex sensory and neurological structures (Baratte & Bonnaud, ; Bassaglia et al, ; Buresi, Baratte, Da Silva, & Bonnaud, ; Buresi, Canali, Bonnaud, & Baratte, ; Buresi, Croll, Tiozzo, Bonnaud, & Baratte, ; Focareta, Sesso, & Cole, ; Zhang & Tublitz, ), as well as muscle (Bassaglia et al, ; Fossati et al, ; Navet et al, ; Zullo et al, ) and endothelium (Focareta & Cole, ). Additional genes of interest should be garnered from the available studies in models across taxa (Fei et al, ; Godwin et al, ; Kawakami et al, ; Uygur & Lee, ; Wischin et al, ); ideally strategies utilizing transcriptomic or single‐cell RNA sequencing could be compared on both amputated and regenerated limb tips to provide greater clarity on intraindividual variation in expression based on injury‐naïve and regenerating conditions.…”