Pax–Six–Eya–Dach network during amphioxus development: Conservation in vitro but context specificity in vivo

Abstract

The Drosophila retinal determination gene network occurs in animals generally as a Pax-Six-Eyes absent-Dachshund network (PSEDN). For amphioxus, we describe the complete network of nine PSEDN genes, four of which-AmphiSix1/2, AmphiSix4/5, AmphSix3/6, and AmphiEya-are characterized here for the first time. For amphioxus, in vitro interactions among the genes and proteins of the network resemble those of other animals, except for the absence of Dach-Eya binding. Amphioxus PSEDN genes are expressed in highly stage- and tissue-specific patterns (sometimes conspicuously correlated with the local intensity of cell proliferation) in the gastrular organizer, notochord, somites, anterior central nervous system, peripheral nervous system, pharyngeal endoderm, and the likely homolog of the vertebrate adenohypophysis. In this last tissue, the anterior region expresses all three amphioxus Six genes and is a zone of active cell proliferation, while the posterior region expresses only AmphiPax6 and is non-proliferative. In summary, the topologies of animal PSEDNs, although considerably more variable than originally proposed, are conserved enough to be recognizable among species and among developing tissues; this conservation may reflect indispensable involvement of PSEDNs during the critically important early phases of embryology (e.g. in the control of mitosis, apoptosis, and cell/tissue motility).

Amphioxus photoreceptors - insights into the evolution of vertebrate opsins, vision and circadian rhythmicity

“…Based on BrdU staining, so-called dorsal compartment motoneurons (probably responsible for control of muscular movements during swimming (Bardet et al, 2005;Wicht and Lacalli, 2005)), located posteriorly to the CV, seem to be differentiated early in development (at midneurula stage), while the neurons of FE are still developing (Holland and Holland 2006). The expression of Pax6 was shown to be exclusive to parts of the CV weakly stained with BrdU, confirming the role of Pax6 in neuronal differentiation in the FE (Kozmik et al, 2007). Our data provide evidence for glutamate immunoreactivity of FE photoreceptors (Fig.…”

“…During the course of development, the expression of Rx and Pax4/6 shifts more posteriorly to Row3 and Row4 cells. Next, expression of Six3/6, the amphioxus orthologue of the vertebrate Six3 and Six6 genes involved in eye development, was documented in the developing FE (Kozmik et al, 2007). Six3/6 and Pax4/6 were shown to be expressed in neurons of the primary motor center (PMC) -anteriormost motoneurons, probably reacting to signals coming from the FE (Kozmik et al, 2007;Vopalensky et al, 2012).…”

“…Next, expression of Six3/6, the amphioxus orthologue of the vertebrate Six3 and Six6 genes involved in eye development, was documented in the developing FE (Kozmik et al, 2007). Six3/6 and Pax4/6 were shown to be expressed in neurons of the primary motor center (PMC) -anteriormost motoneurons, probably reacting to signals coming from the FE (Kozmik et al, 2007;Vopalensky et al, 2012). Based on BrdU staining, so-called dorsal compartment motoneurons (probably responsible for control of muscular movements during swimming (Bardet et al, 2005;Wicht and Lacalli, 2005)), located posteriorly to the CV, seem to be differentiated early in development (at midneurula stage), while the neurons of FE are still developing (Holland and Holland 2006).…”

“…Instead, the area from which the first DO develops expresses Pax2/5/8 during the neurula stage (Kozmik et al, 1999). At later developmental stages scarce Pax2/5/8 (Kozmik et al, 1999) and Dach (Kozmik et al, 2007) expression was detected along the neural tube -whether this expression is localized to differentiating pigment or photoreceptor cells of the subsequently developing DO remains to be determined. Transient expression of Six4/5 and Eya was detected in the amphioxus neurula in two cells in the region where the first DO develops (Kozmik et al, 2007).…”

Novel polyclonal antibodies as a useful tool for expression studies in amphioxus embryos

“…Pax6 encodes a paired and homeobox gene which constitutes a member of the Pax-Six-Eya-Dach network in amphioxus (Kozmik et al, 2007). Pax6 is expressed in the anterior ectoderm from the early neurula stage until the early larval stages (Glardon et al, 1998).…”