Abstract
Cephalopod mollusks possess a number of anatomical traits that often parallel vertebrates in morphological complexity, including a centralized nervous system with sophisticated cognitive functionality. Very little is known about the genetic mechanisms underlying patterning of the cephalopod embryo to arrive at this anatomical structure. Homeodomain (HD) genes are transcription factors that regulate transcription of downstream genes through DNA binding, and as such are integral parts of gene regulatory networks controlling the specification and patterning of body parts across lineages. We have used a degenerate primer strategy to isolate homeobox genes active during late-organogenesis from the European cuttlefish Sepia officinalis. With this approach we have isolated fourteen HD gene fragments and examine the expression profiles of five of these genes during late stage (E24-28) embryonic development (Sof-Gbx, Sof-Hox3, Sof-Arx, Sof-Lhx3/4, Sof-Vsx). All five genes are expressed within the developing central nervous system in spatially restricted and largely non-overlapping domains. Our data provide a first glimpse into the diversity of HD genes in one of the largest, yet least studied, metazoan clades and illustrate how HD gene expression patterns reflect the functional partitioning of the cephalopod brain.
Highlights
Homeodomain (HD) transcription factors are important regulators of developmental patterning across animal lineages, defined by the presence of a 60aa DNA binding homeodomain
Using this strategy we identified 28 amino acids that correspond to amino acids 19–46 of the conserved 60aa homeodomain for four PRD-class HD proteins: dorsal root ganglia homeobox (Sof-Drgx), visual system homeobox (Sof-Vsx), prophet of Pit1 homeobox (SofPropx), and the aristaless-like homeobox (Sof-Arx); and nine ANTP-class HD proteins: gastrulation brain homeobox (Sof-Gbx: new), distalless-like homeobox (Sof-Dlx: new), paralogy group labial/Hox1 (Sof-Hox1: identical to CAI77461.1), paralogy group Hox5/Scr (Sof-Scr: identical to CAI77463.1), paralogy group Hox3 (Sof-Hox3: identical to CAI77462.1), paralogy group ubx/ Lox2/Hox7-8 (Sof-Lox2: new), paralogy group Lox4/Hox8 (SofLox4: identical to CAI77464.1), paralogy group ant/Lox5// Hox6/7 (Sof-Lox5: new), and the ParaHox protein xLox/Pdx (Sof-xLox: new)
We isolate a number of homeobox genes corresponding to the ANTP- PRD- and LIMclasses of HD proteins, profile their expression patterns during the latter half of cephalopod embryogenesis, and report well-defined expression territories that reflect the partitioning of the central nervous system (CNS) into regions with distinct gene signatures (Figure 6)
Summary
Homeodomain (HD) transcription factors are important regulators of developmental patterning across animal lineages, defined by the presence of a 60aa DNA binding homeodomain. The ANTP-class HOX sub-group genes in particular have been widely investigated since the discovery of their conserved role in axial patterning of body plans throughout metazoan lineages [3]. The second largest homeobox gene group is the paired-class (PRD), as defined by the presence of the PRD-homeobox [4]. Where they have been studied, PRD-class genes show expression within developing nervous systems, as well as involvement in axial patterning [5] [6] [7]. It is clear that a number HD transcription factors play a pivotal role in the generation of highly organized central nervous systems
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