Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes

Abstract

Ectodermal placodes comprise the adenohypophyseal, olfactory, lens, profundal, trigeminal, otic, lateral line, and epibranchial placodes. The first part of this review presents a brief overview of placode development. Placodes give rise to a variety of cell types and contribute to many sensory organs and ganglia of the vertebrate head. While different placodes differ with respect to location and derivative cell types, all appear to originate from a common panplacodal primordium, induced at the anterior neural plate border by a combination of mesodermal and neural signals and defined by the expression of Six1, Six4, and Eya genes. Evidence from mouse and zebrafish mutants suggests that these genes promote generic placodal properties such as cell proliferation, cell shape changes, and specification of neurons. The common developmental origin of placodes suggests that all placodes may have evolved in several steps from a common precursor. The second part of this review summarizes our current knowledge of placode evolution. Although placodes (like neural crest cells) have been proposed to be evolutionary novelties of vertebrates, recent studies in ascidians and amphioxus have proposed that some placodes originated earlier in the chordate lineage. However, while the origin of several cellular and molecular components of placodes (e.g., regionalized expression domains of transcription factors and some neuronal or neurosecretory cell types) clearly predates the origin of vertebrates, there is presently little evidence that these components are integrated into placodes in protochordates. A scenario is presented according to which all placodes evolved from an adenohypophyseal-olfactory protoplacode, which may have originated in the vertebrate ancestor from the anlage of a rostral neurosecretory organ (surviving as Hatschek's pit in present-day amphioxus).

Developing a sense of scents: Plasticity in olfactory placode formation

“…These genes along with others [3], appear to be co-expressed in a common region at the anterior end of the neural plate [43]. This region of gene expression correlates with the previously described placode domain (for thorough reviews see [42,43]. Many of the genes expressed in the placode domain are not 5 specific to this region of developing embryos but, like many important developmental transcription factors, are also expressed in other tissues (Six1 and Eya1 in organogenesis and myogenesis for example).…”

“…This unifying theme, namely that all placodes are fundamentally equivalent, also calls to question the basic differences between the peripheral and central nervous system [5]. For example the fact that Six1, Six4 and Eya are all expressed in the placode domain is highlighted as promoting generic placode properties such as cell proliferation, cell shape changes and specification of neurons [42]. Yet these generic properties of placodes are in fact generic properties of the nervous system as a whole.…”

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

“…Although definitive NCCs and placodes did not appear before the emergence of vertebrates, possible evolutionary precursors of these tissues may be present in some invertebrates (Holland and Holland, 1996;Jeffery et al, 2004;reviewed in Bassham et al, 2008;Marlétaz et al, 2006;Schlosser, 2005;Schubert et al, 2006a). It is thus interesting to assess, whether RA signaling affects the development of these invertebrate tissues.…”

How to make a teleost adenohypophysis: Molecular pathways of pituitary development in zebrafish

“…At this phase of development, the neural plate is bordered by the neural crest caudally and the preplacodal ectoderm (ppe) rostrally (Fig.1). Similar to the neural crest, which develops into a variety of cell types like peripheral neurons, glia or pigment cells, the ppe harbors precursors of several tissues, including those of the various sensory ganglia and sensory organs of the head, the inner ear, lenses, olfactory epithelium and the AH (Schlosser, 2005). Within the ppe, these precursors are arranged in a specific spatial pattern, with the future AH cells located in the most anterior domain, the anterior neural ridge (ANR), in close vicinity to the more proximally positioned olfactory precursors and next to the prospective lens cells as their direct posterior neighbors (Dutta et al, 2005).…”