SOXE neofunctionalization and elaboration of the neural crest during chordate evolution.

Andrew Tai,Yong-Heng Huang,Ralf Jauch,Kathryn S E Cheah,Martin Cheung,Marianne E Bronner

doi:10.1038/srep34964

Abstract

During chordate evolution, two genome-wide duplications facilitated acquisition of vertebrate traits, including emergence of neural crest cells (NCCs), in which neofunctionalization of the duplicated genes are thought to have facilitated development of craniofacial structures and the peripheral nervous system. How these duplicated genes evolve and acquire the ability to specify NC and their derivatives are largely unknown. Vertebrate SoxE paralogues, most notably Sox9/10, are essential for NC induction, delamination and lineage specification. In contrast, the basal chordate, amphioxus, has a single SoxE gene and lacks NC-like cells. Here, we test the hypothesis that duplication and divergence of an ancestral SoxE gene may have facilitated elaboration of NC lineages. By using an in vivo expression assay to compare effects of AmphiSoxE and vertebrate Sox9 on NC development, we demonstrate that all SOXE proteins possess similar DNA binding and homodimerization properties and can induce NCCs. However, AmphiSOXE is less efficient than SOX9 in transactivation activity and in the ability to preferentially promote glial over neuronal fate, a difference that lies within the combined properties of amino terminal and transactivation domains. We propose that acquisition of AmphiSoxE expression in the neural plate border led to NCC emergence while duplication and divergence produced advantageous mutations in vertebrate homologues, promoting elaboration of NC traits.

Highlights

During chordate evolution, two genome-wide duplications facilitated acquisition of vertebrate traits, including emergence of neural crest cells (NCCs), in which neofunctionalization of the duplicated genes are thought to have facilitated development of craniofacial structures and the peripheral nervous system
The SOX9-NHMG and AmphiSOXE-NHMG constructs possessing both DIM domain and high-mobility group (HMG) box dimerize substantially more effectively with strong positive cooperativity on CD-Rap and Zero DNA elements (Fig. 3c,d). Both SOX9 and AmphiSOXE bound to and dimerized on DNA in an indistinguishable fashion indicating that they exhibit similar capacity for cooperative binding to the same DNA sequence, despite differences in amino acids within DIM and HMG regions
NC expressing chimeric protein containing the SOX9 HMG box with both the N- and C- domains of AmphiSOXE (E-9-E), differentiated into both neurons and glial (Fig. 6n–p; Supplemental Fig. 5i,j’). These results suggest that N-and C-terminal domains of AmphiSOXE but not the HMG box are responsible for the different influence on neuronal and glial differentiation

Summary

Introduction

Two genome-wide duplications facilitated acquisition of vertebrate traits, including emergence of neural crest cells (NCCs), in which neofunctionalization of the duplicated genes are thought to have facilitated development of craniofacial structures and the peripheral nervous system. The exception is AmphiSNAIL which is expressed in the dorsolateral portion of the amphioxus neural tube, though no neural crest cells arise from this domain[25] This implies that the redeployment of AmphiSoxE gene and/or other ancestral NC-specifiers in the border region may have facilitated emergence of NCCs. Consistent with this, recent studies suggest that such co-option events could have helped to mediate acquisition of NC cis-regulatory sequences in the AmphiSoxE gene[23]. To address whether duplication and divergence of an ancestral SoxE gene may have led to novel functions that facilitated emergence of the NC and its traits in vertebrates, we compared the activity of AmphiSOXE with its vertebrate homologue by analyzing their effects on chicken neural crest development as an assay system

Methods

Results

Conclusion