The Dynamic Regulatory Genome of Capsaspora and the Origin of Animal Multicellularity.
The unicellular ancestor of animals had a complex repertoire of genes linked to multicellular processes. This suggests that changes in the regulatory genome, rather than in gene innovation, were key to the origin of animals. Here, we carry out multiple functional genomic assays in Capsaspora owczarzaki, the unicellular relative of animals with the largest known gene repertoire for transcriptional regulation. We show that changing chromatin states, differential lincRNA expression, and dynamic cis-regulatory sites are associated with life cycle transitions in Capsaspora. Moreover, we demonstrate conservation of animal developmental transcription-factor networks and extensive network interconnection in this premetazoan organism. In contrast, however, Capsaspora lacks animal promoter types, and its regulatory sites are small, proximal, and lack signatures of animal enhancers. Overall, our results indicate that the emergence of animal multicellularity was linked to a major shift in genome cis-regulatory complexity, most notably the appearance of distal enhancer regulation.
Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain. Electronic address: arnau.sebe-pedros@weizmann.ac.il.
Arnau
A
Sebé-Pedrós
Center for Genomic Regulation, Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain.
Cecilia
C
Ballaré
Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
Helena
H
Parra-Acero
Center for Genomic Regulation, Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain.
Cristina
C
Chiva
Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Carretera de Utrera Km1, 41013 Sevilla, Spain.
Juan J
JJ
Tena
Center for Genomic Regulation, Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain.
Eduard
E
Sabidó
Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Carretera de Utrera Km1, 41013 Sevilla, Spain.
José Luis
JL
Gómez-Skarmeta
Center for Genomic Regulation, Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats, Pg Lluis Companys 23, 08010 Barcelona, Spain.
Luciano
L
Di Croce
Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats, Pg Lluis Companys 23, 08010 Barcelona, Spain; Departament de Genètica, Universitat de Barcelona, 08028 Barcelona, Spain. Electronic address: inaki.ruiz@ibe.upf-csic.es.
Iñaki
I
Ruiz-Trillo
D000818:Animals; D005075:Biological Evolution; D056890:Eukaryota / Q000145:classification / Q000166:cytology / Q000235:genetics*; D053263:Gene Regulatory Networks; D016678:Genome; D006657:Histones / Q000378:metabolism; D006801:Humans; D011499:Protein Processing, Post-Translational; D022661:RNA, Untranslated; D050436:Regulatory Elements, Transcriptional
D006657:Histones; D022661:RNA, Untranslated