Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development

Wollesen, Tim, Rodriguez Monje, Sonia Victoria, Todt, Christiane, Degnan, Bernard M. and Wanninger, Andreas (2015) Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development. BMC Evolutionary Biology, 15 10: 1-19. doi:10.1186/s12862-015-0505-z


Author Wollesen, Tim
Rodriguez Monje, Sonia Victoria
Todt, Christiane
Degnan, Bernard M.
Wanninger, Andreas
Title Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development
Formatted title
Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development
Journal name BMC Evolutionary Biology   Check publisher's open access policy
ISSN 1471-2148
Publication date 2015-10-28
Year available 2015
Sub-type Article (original research)
DOI 10.1186/s12862-015-0505-z
Open Access Status DOI
Volume 15
Issue 10
Start page 1
End page 19
Total pages 19
Place of publication London, United Kingdom
Publisher BioMed Central
Collection year 2016
Language eng
Formatted abstract
Background
Mollusks represent the largest lophotrochozoan phylum and exhibit highly diverse body plans. Previous studies have demonstrated that transcription factors such as Pax genes play important roles during their development. Accordingly, in ecdysozoan and vertebrate model organisms, orthologs of Pax2/5/8 are among others involved in the formation of the midbrain/hindbrain boundary, the auditory/geosensory organ systems, and the excretory system.

Methods
Pax2/5/8 expression was investigated by in situ hybridization during the development of representatives of the two major molluscan subclades, Aculifera and Conchifera.

Results
Compared to the investigated polyplacophoran and bivalve species that lack larval statocysts as geosensory organs and elaborate central nervous systems (CNS), cephalopods possess highly centralized brains and statocysts. Pax2/5/8 is expressed in regions where sensory cells develop subsequently during ontogenesis. Expression domains include esthetes and the ampullary system in polyplacophorans as well as the eyes of cephalopods. No Pax2/5/8 expression was observed in the less centralized CNS of bivalve, polyplacophoran, and gastropod embryos, thus arguing for a loss of Pax2/5/8 involvement in CNS development in these lineages. In contrast, Pax2/5/8 is expressed among others in brain lobes along the trajectory of the esophagus that divides the cephalopod brain.

Conclusions
Our results, along with those on Otx- and Hox-gene expression, demonstrate that the cephalopod condition is similar to that in mouse and fruit fly, with Otx being expressed in the anterior-most brain region (except for the vertical lobe) and a Pax2/5/8 expression domain separating the Otx-domain from a Hox-gene expressing posterior brain region. Thus, Pax2/5/8 appears to have been recruited independently into regionalization of non-homologous complex brains of organisms as different as squid, fruit fly, and mouse. In addition, Pax2/5/8 is expressed in multimodal sensory systems in mollusks such as the esthetes and the ampullary system of polyplacophorans as well as the eyes of cephalopods. Pax2/5/8-expressing cells are present in regions where the future sensory cells such as the polyplacophoran esthetes are situated and hence Pax2/5/8 expression probably predates sensory cell development during ontogeny. In mollusks, Pax2/5/8 is only expressed in derivatives of the ectoderm and hence an ancestral role in molluscan ectoderm differentiation is inferred.
Keyword Bivalvia
Cephalopod
Complexity
Evolution
Homeobox
Hox
Lophotrochozoa
Neurogenesis
Sensory cell
Polyplacophora
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2016 Collection
School of Biological Sciences Publications
 
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