Co-option of the limb patterning program in cephalopod eye development

Stephanie Neal,Kyle J Mcculloch,Christina M Daly,Kristen M Koenig,Francesca R Napoli,James H Coleman

doi:10.1186/s12915-021-01182-2

Stephanie Neal, Kyle J Mcculloch + Show 4 more

Open Access

https://doi.org/10.1186/s12915-021-01182-2

Copy DOI

Journal: BMC biology	Publication Date: Jan 5, 2022
Citations: 34	License type: open-access

Affiliation: Harvard University Press, Harvard University

Abstract

BackgroundAcross the Metazoa, similar genetic programs are found in the development of analogous, independently evolved, morphological features. The functional significance of this reuse and the underlying mechanisms of co-option remain unclear. Cephalopods have evolved a highly acute visual system with a cup-shaped retina and a novel refractive lens in the anterior, important for a number of sophisticated behaviors including predation, mating, and camouflage. Almost nothing is known about the molecular-genetics of lens development in the cephalopod.ResultsHere we identify the co-option of the canonical bilaterian limb patterning program during cephalopod lens development, a functionally unrelated structure. We show radial expression of transcription factors SP6-9/sp1, Dlx/dll, Pbx/exd, Meis/hth, and a Prdl homolog in the squid Doryteuthis pealeii, similar to expression required in Drosophila limb development. We assess the role of Wnt signaling in the cephalopod lens, a positive regulator in the developing Drosophila limb, and find the regulatory relationship reversed, with ectopic Wnt signaling leading to lens loss.ConclusionThis regulatory divergence suggests that duplication of SP6-9 in cephalopods may mediate the co-option of the limb patterning program. Thus, our study suggests that this program could perform a more universal developmental function in radial patterning and highlights how canonical genetic programs are repurposed in novel structures.

Highlights

In the Metazoa, homologous networks of transcription factors are necessary for the development of some analogous structures in distantly related taxa
Proximal-distal limb patterning genes in the anterior segment of the cephalopod To assess whether genes involved in appendage patterning may be required for cephalopod lens development, we identified and performed in situ hybridization for the genes Dlx, Meis, Pbx, and Dac at stages 21 and 23 (Fig. 2, Supplemental Figure 2, Supplemental Figure 3)
This change in signaling and the known duplication of SP6-9 and the novel expression of the SP6-9a paralog in the anterior segment suggests that this duplication may be a mediator of limb patterning program co-option in the anterior segment

Summary

Introduction

Background In the Metazoa, homologous networks of transcription factors are necessary for the development of some analogous structures in distantly related taxa. The transcription factor SP6-9/sp is upstream of other program members, Dlx/dll, Pbx/exd, Meis/hth, Dac, and Arx/ar, each required for patterning specific regions of limb outgrowth [3,4,5,6,7,8,9] This network is necessary in both vertebrate and cephalopod limb development and is expressed in a similar proximodistal pattern in a diversity of outgrowths [1, 3, 5, 10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25]. Almost nothing is known about the molecular-genetics of lens development in the cephalopod

Methods

Results

Conclusion