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Èlia Benito‐Gutiérrez

University of Cambridge

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Jordi García‐Fernàndez

Universitat de Barcelona

Giacomo Gattoni

Columbia University

Michael Schubert

Laboratoire de Biologie du Développement de Villefranche-sur-Mer

Detlev Arendt

European Molecular Biology Laboratory

Ricard Albalat

Universitat de Barcelona

Vincent Laudet

Okinawa Institute of Science and Technology Graduate University

Mario Pestarino

University of Genoa

Toby G. R. Andrews

The Francis Crick Institute

Simona Candiani

University of Genoa

Daniel Keitley

University of Cambridge

Cooperative Institutions

Centre National de la Recherche Scientifique

University of Cambridge

Universitat de Barcelona

University of California, Berkeley

Sorbonne Université

Joint Genome Institute

Kyoto University

The University of Tokyo

European Molecular Biology Laboratory

University College London

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The amphioxus genome illuminates vertebrate origins and cephalochordate biology (Genome Research (2008) 18, (1100-1111))

Genome Research (2008)

Linda Z. Holland Ricard Albalat Kaoru Azumi Èlia Benito‐Gutiérrez Matthew J. Blow

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Citations (0)

Hybridization Chain Reaction for Quantitative and Multiplex Imaging of Gene Expression in Amphioxus Embryos and Adult Tissues

Methods in molecular biology (2020)

Toby G. R. Andrews Giacomo Gattoni Lara Busby Michael A. Schwimmer Èlia Benito‐Gutiérrez

Chordate

Multiplex

10.1007/978-1-0716-0623-0_11

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Citations (14)

Mirnovo: genome-free prediction of microRNAs from small RNA sequencing data and single-cells using decision forests

Nucleic Acids Research (2017)

Dimitrios Vitsios Elissavet Kentepozidou Leonor Quintais Èlia Benito‐Gutiérrez Stijn van Dongen

The discovery of microRNAs (miRNAs) remains an important problem, particularly given the growth of high-throughput sequencing, cell sorting and single cell biology. While a large number of miRNAs have already been annotated, there may well be large numbers of miRNAs that are expressed in very particular cell types and remain elusive. Sequencing allows us to quickly and accurately identify the expression of known miRNAs from small RNA-Seq data. The biogenesis of miRNAs leads to very specific characteristics observed in their sequences. In brief, miRNAs usually have a well-defined 5' end and a more flexible 3' end with the possibility of 3' tailing events, such as uridylation. Previous approaches to the prediction of novel miRNAs usually involve the analysis of structural features of miRNA precursor hairpin sequences obtained from genome sequence. We surmised that it may be possible to identify miRNAs by using these biogenesis features observed directly from sequenced reads, solely or in addition to structural analysis from genome data. To this end, we have developed mirnovo, a machine learning based algorithm, which is able to identify known and novel miRNAs in animals and plants directly from small RNA-Seq data, with or without a reference genome. This method performs comparably to existing tools, however is simpler to use with reduced run time. Its performance and accuracy has been tested on multiple datasets, including species with poorly assembled genomes, RNaseIII (Drosha and/or Dicer) deficient samples and single cells (at both embryonic and adult stage).

Drosha

Dicer

MiRBase

10.1093/nar/gkx836

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Citations (64)

Amphioxus as a Model for Mechanisms in Vertebrate Development

Encyclopedia of Life Sciences (2011)

Èlia Benito‐Gutiérrez

Abstract For the last two centuries, the cephalochordates, commonly known as lancelets or amphioxus, have been central to investigate the evolutionary genesis of vertebrates. At first, by classical morphologists fascinated by their odd but at the same time familiar anatomical traits and later by molecular biologists giving the first insights into their slow evolving nature. The present data available not only holds amphioxus as an organism of preternatural importance within the tree of life but also boosts its potential to untangle the molecular basis underlying the vertebrate complexity. This is a walk through the past and present of the amphioxus field merging morphological and molecular data in linkage with the fossil record and the modern vertebrates. The resulting picture is drawn together with comparative maps of genome organisation, gastrulation and the origin of the vertebrate organiser, neurulation and the origin of the neural crest, and shared signalling mechanisms between vertebrates and amphioxus during development. Special attention is also given to some of the most critical vertebrate novelties and how the pre‐duplicative amphioxus genetic toolkit might have contributed to set the basis for evolving complexity in the course of vertebrate evolution. Key Concepts: Cephalochordates occupy at present the key phylogenetic position to get insights into the invertebrate–vertebrate transition and the evolutionary genesis of vertebrates. Whole‐genome duplications in the lineage leading to modern vertebrates might have established the basis for molecular and morphological innovation. The amphioxus genome appears to be the best surrogate available for the ancestral chordate genome regarding the gene content, gene structure and chromosomal organisation. The amphioxus prototypical body plan with respect to vertebrates facilitates the comparative analysis and linkage between invertebrates and vertebrates. The pre‐duplicative genome of amphioxus offers the possibility of analysing vertebrate‐like gene regulatory networks in a simpler biological context with a reduced number of molecular players.

Chordate

Evolutionary developmental biology

Lineage (genetic)

Amniote

10.1002/9780470015902.a0021773

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Citations (4)

A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Jenaid Rees Katie Kirk Giacomo Gattoni Dorit Hockman Dylan Ritter

Summary Vertebrate calcitonin-producing cells (C-cells) are neuroendocrine cells that secrete the small peptide hormone calcitonin in response to elevated blood calcium levels. C-cells are crucial for maintenance of calcium homeostasis, yet the embryonic and evolutionary origins of this cell type remain contentious. Whereas mouse C-cells reside within the thyroid gland and derive from pharyngeal endoderm, avian C-cells are located within ultimobranchial glands and were reported to derive from the neural crest. We use a comparative cell lineage tracing approach in a range of vertebrate model systems to resolve the ancestral embryonic origin of vertebrate C-cells. We find, contrary to previous studies, that chick C-cells derive from pharyngeal endoderm, with neural crest-derived cells instead contributing to connective tissue intimately associated with C-cells in the ultimobranchial gland. This endodermal origin of C-cells is conserved in a ray-finned bony fish (zebrafish) and a cartilaginous fish (the little skate, Leucoraja erinacea ). Furthermore, we discover putative C-cell homologues within the endodermally-derived pharyngeal epithelium of the ascidian Ciona intestinalis and the amphioxus Branchiostoma lanceolatum , two invertebrate chordates that lack neural crest cells. Our findings point to a conserved endodermal origin of C-cells across vertebrates and to a pre-vertebrate origin of this cell type along the chordate stem.

Chordate

Ciona

Hagfish

Cell type

Septate junctions

10.1101/2024.02.17.580846

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Citations (1)

A gene catalogue of the amphioxus nervous system

International Journal of Biological Sciences (2006)

Èlia Benito‐Gutiérrez

The elaboration of extremely complex nervous systems is a major success of evolution.However, at the dawn of the post-genomic era, few data have helped yet to unravel how a nervous system develops and evolves to complexity.On the evolutionary road to vertebrates, amphioxus occupies a key position to tackle this exciting issue.Its "simple" nervous system basically consists of a dorsal nerve cord and a diffuse net of peripheral neurons, which contrasts greatly with the complexity of vertebrate nervous systems.Notwithstanding, increasing data on gene expression has faced up this simplicity by revealing a mounting level of cryptic complexity, with unexpected levels of neuronal diversity, organisation and regionalisation of the central and peripheral nervous systems.Furthermore, recent gene expression data also point to the high neurogenic potential of the epidermis of amphioxus, suggestive of a skin-brain track for the evolution of the vertebrate nervous system.Here I attempt to catalogue and synthesise current gene expression data in the amphioxus nervous system.From this global point of view, I suggest scenarios for the evolutionary origin of complex features in the vertebrate nervous system, with special emphasis on the evolutionary origin of placodes and neural crest, and postulate a pre-patterned migratory pathway of cells, which, in the epidermis, may represent an intermediate state towards the deployment of one of the most striking innovative features of vertebrates: the neural crest and its derivatives.

Chordate

10.7150/ijbs.2.149

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Citations (21)

The dorsoanterior brain of adult amphioxus shares similarities in expression profile and neuronal composition with the vertebrate telencephalon

BMC Biology (2021)

Èlia Benito‐Gutiérrez Giacomo Gattoni Manuel Stemmer Silvia D. Rohr Laura Schuhmacher

The evolutionary origin of the telencephalon, the most anterior part of the vertebrate brain, remains obscure. Since no obvious counterpart to the telencephalon has yet been identified in invertebrate chordates, it is difficult to trace telencephalic origins. One way to identify homologous brain parts between distantly related animal groups is to focus on the combinatorial expression of conserved regionalisation genes that specify brain regions.

10.1186/s12915-021-01045-w

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Citations (26)

The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells

Development (2005)

Èlia Benito‐Gutiérrez Christian Näke Marta Llovera Joan X. Comella Jordi García‐Fernàndez

Neurotrophins (Nt) and their tyrosine kinase Trk receptors play an essential role in the development and maintenance of the complex vertebrate nervous system. Invertebrate genome sequencing projects have suggested that the Nt/Trk system is a vertebrate innovation. We describe the isolation and characterisation of the amphioxus Trk receptor, AmphiTrk. Its ancestral link to vertebrate Trk receptors is supported by phylogenetic analysis and domain characterisation. The genomic structure of AmphiTrk strongly suggests that a ProtoTrk gene emerged by means of exon-shuffling prior to the cephalochordate/vertebrate split. We also examined the physiological response of AmphiTrk to vertebrate neurotrophins,and found that despite 500 million years of divergence, AmphiTrk transduces signals mediated by NGF, BDNF, NT3 and NT4. Markedly, AmphiTrk is able to activate survival and differentiation pathways, but fails to activate the PLCγ pathway, which is involved in synaptic plasticity in higher vertebrates. AmphiTrk is expressed during amphioxus embryogenesis in sensory neural precursors in the epidermis, which possesses single migratory cells. We propose that the duplication and divergence of the Nt/Trk system, in tandem with recruitment of the PLCγ pathway, may have provided the genetic basis for a key aspect of vertebrate evolution: the complexity of the nervous system.

Signalling

Signalling pathways

10.1242/dev.01803

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Citations (68)

Methods for Generating Year-Round Access to Amphioxus in the Laboratory

PLoS ONE (2013)

Èlia Benito‐Gutiérrez Hermann Weber Diana Virginia Bryant Detlev Arendt

Cephalochordates, commonly known as amphioxus, are key to understanding vertebrate origins. However, laboratory work suffers from limited access to adults and embryonic material. Here we report the design and experimental validation of an inland marine facility that allows establishing stable amphioxus colonies in the laboratory and obtaining embryos at any time of day and over almost the entire year, far exceeding natural conditions. This is achieved by mimicking the natural benthic environment, natural day- and moon- light, natural substrate and by providing a strictly controlled and seasonally fluctuating temperature regimen. Moreover, supplemented algae diets allow animals to refill their gonads in consecutive years. Spontaneous spawning, a major problem in previous setups, no longer occurs in our facility; instead, all breeding is induced and fertilization occurs fully in vitro. Our system makes amphioxus a standard laboratory animal model.

10.1371/journal.pone.0071599

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Citations (25)

Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye

Proceedings of the National Academy of Sciences (2012)

Pavel Vopálenský Jiří Pergner Michaela Liegertová Èlia Benito‐Gutiérrez Detlev Arendt

The origin of vertebrate eyes is still enigmatic. The “frontal eye” of amphioxus, our most primitive chordate relative, has long been recognized as a candidate precursor to the vertebrate eyes. However, the amphioxus frontal eye is composed of simple ciliated cells, unlike vertebrate rods and cones, which display more elaborate, surface-extended cilia. So far, the only evidence that the frontal eye indeed might be sensitive to light has been the presence of a ciliated putative sensory cell in the close vicinity of dark pigment cells. We set out to characterize the cell types of the amphioxus frontal eye molecularly, to test their possible relatedness to the cell types of vertebrate eyes. We show that the cells of the frontal eye specifically coexpress a combination of transcription factors and opsins typical of the vertebrate eye photoreceptors and an inhibitory Gi-type alpha subunit of the G protein, indicating an off-responding phototransductory cascade. Furthermore, the pigmented cells match the retinal pigmented epithelium in melanin content and regulatory signature. Finally, we reveal axonal projections of the frontal eye that resemble the basic photosensory-motor circuit of the vertebrate forebrain. These results support homology of the amphioxus frontal eye and the vertebrate eyes and yield insights into their evolutionary origin.

Chordate

Opsin

Eye Proteins

Forebrain

10.1073/pnas.1207580109

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Citations (124)