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Amphioxus functional genomics and the origins of vertebrate gene regulation.

ABSTRACT: Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that-in vertebrates-over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.

SUBMITTER: Marletaz F

PROVIDER: S-EPMC6292497 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Amphioxus functional genomics and the origins of vertebrate gene regulation.

Marlétaz Ferdinand F Firbas Panos N PN Maeso Ignacio I Tena Juan J JJ Bogdanovic Ozren O Perry Malcolm M Wyatt Christopher D R CDR de la Calle-Mustienes Elisa E Bertrand Stephanie S Burguera Demian D Acemel Rafael D RD van Heeringen Simon J SJ Naranjo Silvia S Herrera-Ubeda Carlos C Skvortsova Ksenia K Jimenez-Gancedo Sandra S Aldea Daniel D Marquez Yamile Y Buono Lorena L Kozmikova Iryna I Permanyer Jon J Louis Alexandra A Albuixech-Crespo Beatriz B Le Petillon Yann Y Leon Anthony A Subirana Lucie L Balwierz Piotr J PJ Duckett Paul Edward PE Farahani Ensieh E Aury Jean-Marc JM Mangenot Sophie S Wincker Patrick P Albalat Ricard R Benito-Gutiérrez Èlia È Cañestro Cristian C Castro Filipe F D'Aniello Salvatore S Ferrier David E K DEK Huang Shengfeng S Laudet Vincent V Marais Gabriel A B GAB Pontarotti Pierre P Schubert Michael M Seitz Hervé H Somorjai Ildiko I Takahashi Tokiharu T Mirabeau Olivier O Xu Anlong A Yu Jr-Kai JK Carninci Piero P Martinez-Morales Juan Ramon JR Crollius Hugues Roest HR Kozmik Zbynek Z Weirauch Matthew T MT Garcia-Fernàndez Jordi J Lister Ryan R Lenhard Boris B Holland Peter W H PWH Escriva Hector H Gómez-Skarmeta Jose Luis JL Irimia Manuel M

Nature 20181121 7734

Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebra ...[more]

PMID: 30464347

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Project description:BackgroundA common feature of chemosensory systems is the involvement of G protein-coupled receptors (GPCRs) in the detection of environmental stimuli. Several lineages of GPCRs are involved in vertebrate olfaction, including trace amine-associated receptors, type 1 and 2 vomeronasal receptors and odorant receptors (ORs). Gene duplication and gene loss in different vertebrate lineages have lead to an enormous amount of variation in OR gene repertoire among species; some fish have fewer than 100 OR genes, while some mammals possess more than 1000. Fascinating features of the vertebrate olfactory system include allelic exclusion, where each olfactory neuron expresses only a single OR gene, and axonal guidance where neurons expressing the same receptor project axons to common glomerulae. By identifying homologous ORs in vertebrate and in non-vertebrate chordates, we hope to expose ancestral features of the chordate olfactory system that will help us to better understand the evolution of the receptors themselves and of the cellular components of the olfactory system.ResultsWe have identified 50 full-length and 11 partial ORs in Branchiostoma floridae. No ORs were identified in Ciona intestinalis. Phylogenetic analysis places the B. floridae OR genes in a monophyletic clade with the vertebrate ORs. The majority of OR genes in amphioxus are intronless and many are also tandemly arrayed in the genome. By exposing conserved amino acid motifs and testing the ability of those motifs to discriminate between ORs and non-OR GPCRs, we identified three OR-specific amino acid motifs common in cephalochordate, fish and mammalian and ORs.ConclusionHere, we show that amphioxus has orthologs of vertebrate ORs. This conclusion demonstrates that the receptors, and perhaps other components of vertebrate olfaction, evolved at least 550 million years ago. We have also identified highly conserved amino acid motifs that may be important for maintaining receptor conformation or regulating receptor activity. We anticipate that the identification of vertebrate OR orthologs in amphioxus will lead to an improved understanding of OR gene family evolution, OR gene function, and the mechanisms that control cell-specific expression, axonal guidance, signal transduction and signal integration.

Project description:Classically, the estrogen signaling system has two core components: cytochrome P450 aromatase (CYP19), the enzyme complex that catalyzes the rate limiting step in estrogen biosynthesis; and estrogen receptors (ERs), ligand activated transcription factors that interact with the regulatory region of target genes to mediate the biological effects of estrogen. While the importance of estrogens for regulation of reproduction, development and physiology has been well-documented in gnathostome vertebrates, the evolutionary origins of estrogen as a hormone are still unclear. As invertebrates within the phylum Chordata, cephalochordates (e.g., the amphioxus of the genus Branchiostoma) are among the closest invertebrate relatives of the vertebrates and can provide critical insight into the evolution of vertebrate-specific molecules and pathways. To address this question, this paper briefly reviews relevant earlier studies that help to illuminate the history of the aromatase and ER genes, with a particular emphasis on insights from amphioxus and other invertebrates. We then present new analyses of amphioxus aromatase and ER sequence and function, including an in silico model of the amphioxus aromatase protein, and CYP19 gene analysis. CYP19 shares a conserved gene structure with vertebrates (9 coding exons) and moderate sequence conservation (40% amino acid identity with human CYP19). Modeling of the amphioxus aromatase substrate binding site and simulated docking of androstenedione in comparison to the human aromatase shows that the substrate binding site is conserved and predicts that androstenedione could be a substrate for amphioxus CYP19. The amphioxus ER is structurally similar to vertebrate ERs, but differs in sequence and key residues of the ligand binding domain. Consistent with results from other laboratories, amphioxus ER did not bind radiolabeled estradiol, nor did it modulate gene expression on an estrogen-responsive element (ERE) in the presence of estradiol, 4-hydroxytamoxifen, diethylstilbestrol, bisphenol A or genistein. Interestingly, it has been shown that a related gene, the amphioxus "steroid receptor" (SR), can be activated by estrogens and that amphioxus ER can repress this activation. CYP19, ER and SR are all primarily expressed in gonadal tissue, suggesting an ancient paracrine/autocrine signaling role, but it is not yet known how their expression is regulated and, if estrogen is actually synthesized in amphioxus, whether it has a role in mediating any biological effects. Functional studies are clearly needed to link emerging bioinformatics and in vitro molecular biology results with organismal physiology to develop an understanding of the evolution of estrogen signaling. This article is part of a Special Issue entitled 'Marine organisms'.

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Amphioxus functional genomics and the origins of vertebrate gene regulation.

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Amphioxus functional genomics and the origins of vertebrate gene regulation.

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