Regulatory principles of echinoderm metamorphosis
Lead Research Organisation:
University College London
Department Name: Genetics Evolution and Environment
Abstract
While some animals develop directly from embryos into their adult forms, others present an intermediate larval stage. The metamorphosis of the larva into the adult form can be more or less dramatic, and, in the case of echinoderms, involve a drastic change in body symmetry from a bilateral larva into a pentaradial adult (five-way symmetry). The adult first grows as a set of cells, the 'rudiment' that grows within the larva and finally everts from it. While this process relies on the same development genes as embryonic development, these genes are mobilised by an alternative developmental program encoded in the genome. I want to understand how these two regulatory programs that control development from egg to larva and from larva to pentaradial adult can coexist in the same genome.
Genes are controlled by regulatory elements, segments of DNA that are bound by specialised proteins called transcription factors. I want to determine what are the regulatory elements in the genome that control the metamorphosis of the larval into an adult with an alternative body symmetry and which transcription factors play the most important role in mobilising these elements. We will use sequencing-based technologies, such as single-cell transcriptomics and computational analyses to find this out. We will then use transgenic sea urchin larvae carrying a gene encoding for a fluorescent protein under the control of such promoters to monitor where these regulatory elements are active.
Echinoderm genomes are quite plastic, which means gene order can change and some have postulated that this could have played a key role in rewiring gene regulation. To test this idea, we will evaluate the genomic changes that took place in different echinoderm lineages. Then, as regulatory elements are embedded in loops of DNA known as three-dimensional chromatin compartments, we will see if these are affected during metamorphosis, and finally build an integrative model of rudiment development. We expect to uncover the new regulatory route that has made possible the evolution of a new body plan in these mesmerising organisms.
Genes are controlled by regulatory elements, segments of DNA that are bound by specialised proteins called transcription factors. I want to determine what are the regulatory elements in the genome that control the metamorphosis of the larval into an adult with an alternative body symmetry and which transcription factors play the most important role in mobilising these elements. We will use sequencing-based technologies, such as single-cell transcriptomics and computational analyses to find this out. We will then use transgenic sea urchin larvae carrying a gene encoding for a fluorescent protein under the control of such promoters to monitor where these regulatory elements are active.
Echinoderm genomes are quite plastic, which means gene order can change and some have postulated that this could have played a key role in rewiring gene regulation. To test this idea, we will evaluate the genomic changes that took place in different echinoderm lineages. Then, as regulatory elements are embedded in loops of DNA known as three-dimensional chromatin compartments, we will see if these are affected during metamorphosis, and finally build an integrative model of rudiment development. We expect to uncover the new regulatory route that has made possible the evolution of a new body plan in these mesmerising organisms.
Technical Summary
While some animals develop directly from embryos into their adult forms, others present an intermediate larval stage. The metamorphosis of the larva into the adult form can be more or less drastic, and, in the case of echinoderms, involve a change in body symmetry from a bilateral larva into a pentaradial adult (five-way symmetry). The adult first grows as a set of cells, the 'rudiment' that grows within the larva and finally everts from it. While this process relies on the same development genes as embryonic development, these genes are mobilised by an alternative developmental program encoded in the genome. I want to understand how these two regulatory programs (the embryonic and metamorphosis ones) can coexist in the genome and be successively activated, by better understanding the regulatory architecture of echinoderm genomes. To do this, I first want to characterise the regulatory elements involved in rudiment development, identify the key transcription factors responsible for the initiation of the rudiment development and functionally assess their role. Then, I plan to experimentally survey the activation pattern of rudiment specific elements using a reporter approach and dissect their combinatorial and respective role in establishing a pentaradial bodyplan. Finally, I will investigate how the genome plasticity of echinoderms has reshaped their regulatory architecture by combining comparative genomics with HiC to characterise three-dimensional chromatin domains controlling rudiment regulation. We expect to uncover the new regulatory route that has made possible the evolution of a new bodyplan in these mesmerising organisms.
Publications
Brasó-Vives M
(2022)
Parallel evolution of amphioxus and vertebrate small-scale gene duplications.
in Genome biology
Finet C
(2021)
DrosoPhyla: Resources for Drosophilid Phylogeny and Systematics.
in Genome biology and evolution
Marlétaz F
(2023)
Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes.
in Cell genomics
Marlétaz F
(2023)
The little skate genome and the evolutionary emergence of wing-like fins.
in Nature
Marlétaz F
(2023)
The hagfish genome and the evolution of vertebrates
Martín-Durán JM
(2021)
Publisher Correction: Conservative route to genome compaction in a miniature annelid.
in Nature ecology & evolution
Martín-Durán JM
(2021)
Conservative route to genome compaction in a miniature annelid.
in Nature ecology & evolution
Martín-Zamora FM
(2023)
Annelid functional genomics reveal the origins of bilaterian life cycles.
in Nature
Miryeganeh M
(2022)
De novo genome assembly and in natura epigenomics reveal salinity-induced DNA methylation in the mangrove tree Bruguiera gymnorhiza.
in The New phytologist
Piovani L
(2023)
Single-cell transcriptomics refuels the exploration of spiralian biology.
in Briefings in functional genomics
Description | Collaboration |
Organisation | Queen Mary University of London |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Collaboration with Alex de Mendoza about epigenetic during animal development |
Collaborator Contribution | very meaningful chats |
Impact | interesting ideas |
Start Year | 2022 |
Description | Setting up a new urchin model |
Organisation | Horniman Museum and Gardens |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | This is a collaboration with Jamie Craggs at the Horniman museum to develop the tuxedo urchin Mespilia globosa as a promising model. |
Collaborator Contribution | Providing advice about culture of urchin and lava and also animals larvae. |
Impact | The museum aquarium has an opportunity to reach the public, possible future outreach options will be considered. The partner has exceptional expertise in rearing of tropical marine invertebrates. |
Start Year | 2021 |