Emergence of novel genomic regulatory regions associated with light-organ development in the bobtail squid
Lisa Rouressol,
John Briseno,
Nidhi Vijayan,
Grischa Y. Chen,
Elena A. Ritschard,
Gustavo Sanchez,
Spencer V. Nyholm,
Margaret J. McFall-Ngai,
Oleg Simakov
Affiliations
Lisa Rouressol
Department for Neurosciences and Developmental Biology, University of Vienna, Vienna 1030, Austria; Department of Biosphere Sciences and Engineering, Carnegie Institution for Science, Pasadena, CA 91125, USA; Corresponding author
John Briseno
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA
Nidhi Vijayan
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA
Grischa Y. Chen
Department of Biosphere Sciences and Engineering, Carnegie Institution for Science, Pasadena, CA 91125, USA
Elena A. Ritschard
Department for Neurosciences and Developmental Biology, University of Vienna, Vienna 1030, Austria; Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, 80121 Napoli, NA, Italy
Gustavo Sanchez
Molecular Genetics Unit, Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan
Spencer V. Nyholm
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA
Margaret J. McFall-Ngai
Department of Biosphere Sciences and Engineering, Carnegie Institution for Science, Pasadena, CA 91125, USA; Corresponding author
Oleg Simakov
Department for Neurosciences and Developmental Biology, University of Vienna, Vienna 1030, Austria; Corresponding author
Summary: Light organs (LO) with symbiotic bioluminescent bacteria are hallmarks of many bobtail squid species. These organs possess structural and functional features to modulate light, analogous to those found in coleoid eyes. Previous studies identified four transcription factors and modulators (SIX, EYA, PAX6, DAC) associated with both eyes and light organ development, suggesting co-option of a highly conserved gene regulatory network. Using available topological, open chromatin, and transcriptomic data, we explore the regulatory landscape around the four transcription factors as well as genes associated with LO and shared LO/eye expression. This analysis revealed several closely associated and putatively co-regulated genes. Comparative genomic analyses identified distinct evolutionary origins of these putative regulatory associations, with the DAC locus showing a unique topological and evolutionarily recent organization. We discuss different scenarios of modifications to genome topology and how these changes may have contributed to the evolutionary emergence of the light organ.
