Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

Marlétaz, Ferdinand; Couloux, Arnaud; Poulain, Julie; Labadie, Karine; Silva, Corinne Da; Mangenot, Sophie; Noël, Benjamin; Poustka, Albert J.; Dru, Philippe; Pegueroles, Cinta; Borra, Marco; Lowe, Elijah K.; Lhomond, Guy; Besnardeau, Lydia; Gras, Stéphanie Le; Ye, Tao; Gavriouchkina, Daria; Russo, Roberta; Costa, Caterina; Zito, Francesca; Anello, Letizia; Nicosia, Aldo; Ragusa, Maria Antonietta; Pascual, Marta; Molina, Maria Dolores; Chessel, Aline; Carlo, Marta Di; Turon, Xavier; Copley, Richard R.; Exposito, Jean‐Yves; Martı́nez, Pedro; Cavalieri, Vincenzo; Leon, Smadar Ben Tabou de; Croce, Jenifer C.; Oliveri, Paola; Matranga, Valeria; Bernardo, Maria Di; Morales, Julia; Geneviève, Anne-Marie; Aury, Jean‐Marc; Barbe, Valérie; Wincker, Patrick; Arnone, Maria Ina; Gache, Christian; Lepage, Thierry

doi:10.1016/j.xgen.2023.100295

Cited by 28 publications

(36 citation statements)

References 119 publications

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“…10). These two fusions were also observed in the recently decoded sea urchin P. lividus genome 24 , indicating a common genomic trait of currently available sea urchin genomes. We also deduced 20 ALGs (LALGs) in the Lytechinus LCA, owing to a Lytechinus -specific chromosomal fusion event (G●D) (node L in Supplementary Fig.…”

Section: Resultssupporting

confidence: 52%

“…The inferred chordate-specific chromosomal dispersion and the four chromosomal fusion events in amphioxus BFL are consistent with previous findings 18 . One of these fusion events (A1⊗A2) was also observed in the sea urchin Paracentrotus lividus 24 , suggesting that A1 and A2 were arms of a metacentric chromosome that fused independently in urchin and amphioxus. From the 23 chordate ALGs, previous studies 18, 19 deduced that the lineage leading to vertebrates had undergone four chromosomal fusion events (J1⊗J2, C1⊗C2, O1⊗O2 and B1⊗B2⊗B3), reducing the 23 CALGs to 18 vertebrate ALGs.…”

Section: Resultsmentioning

confidence: 83%

“…In the sea urchin S. purpuratus , SPU8 chromosome arose through the fusion of EALGs J1 and B3, via central insertion (J1↘B3), while SPU1 arose by fusion with extensively mixing from EALGs E and B2⊗C2, denoted as E⊗(B2⊗C2), resulting in 1 N =21 chromosomes. The three-way fusion E⊗(B2⊗C2), is also shared by Lytechinus variegatus 18 and Paracentrotus lividus 24 , and is therefore likely a shared derived character of the superorder Echinacea, a hypothesis that can be tested by sequencing other members of this group.…”

Section: Resultsmentioning

confidence: 99%

“…For S. californicum , gene prediction was performed as in Marlétaz et al 2023 24 . Briefly, hints for de novo prediction using Augustus 71 were derived from transcriptome and protein alignments.…”

Section: Methodsmentioning

confidence: 99%

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Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

Lin,

Marlétaz,

Pérez-Posada

et al. 2023

Preprint

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Deuterostomes are an animal superphylum that includes Hemichordata and Echinodermata (together Ambulacraria) and Chordata. The diversity of deuterostome body plans has made it challenging to reconstruct their ancestral condition and to decipher the genetic changes that drove the diversification of deuterostome lineages. Here, we generate chromosome-level genome assemblies of two hemichordate species,Ptychodera flavaandSchizocardium californicum, and use comparative genomic approaches to infer the chromosomal architecture of the deuterostome common ancestor and delineate lineage-specific chromosomal modifications. We show that hemichordate chromosomes (1N=23) exhibit remarkable chromosome-scale macrosynteny when compared to other deuterostomes, and can be derived from 24 deuterostome ancestral linkage groups (ALGs). These deuterostome ALGs in turn match previously inferred bilaterian ALGs, consistent with a relatively short transition from the last common bilaterian ancestor to the origin of deuterostomes. Based on this deuterostome ALG complement, we deduced chromosomal rearrangement events that occurred in different lineages. For example, a fusion-with-mixing event produced an Ambulacraria-specific ALG that subsequently split into two chromosomes in extant hemichordates, while this homologous ALG further fused with another chromosome in sea urchins. Orthologous genes distributed in these rearranged chromosomes are enriched for functions in various developmental processes. We found that the deeply conserved Hox clusters are located in highly rearranged chromosomes but have lower densities of transposable elements within the clusters. We also provide evidence that the deuterostome-specific pharyngeal gene cluster was established via the combination of three pre-assembled microsyntenic blocks. We suggest that since chromosomal rearrangement events and formation of new gene clusters may change the regulatory controls of developmental genes, these events may have contributed to the evolution of diverse body plans among deuterostomes.

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Section: Resultssupporting

confidence: 52%

Section: Resultsmentioning

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

Lin,

Marlétaz,

Pérez-Posada

et al. 2023

Preprint

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“…The detailed features of genome sequences of various organisms promote the research for a variety of universal and specific activities of the entire living systems. Therefore, as similar to various organisms, sea urchins draft genomes were also assembled; for example Sp in 2006 (Sodergren et al, 2006) (the latest version was updated in 2019), H. pulcerrimus in 2018 (Kinjo, Kiyomoto, Yamamoto, Ikeo, & Yaguchi, 2018), Lytechinus variegatus in 2020 (P. L. Davidson et al, 2020), Temnopleurus reevesii in 2022 (Kinjo et al, 2022), and Paracentrotus lividus in 2023 (Marletaz, Couloux, & Poulain, 2023).…”

Section: Introductionmentioning

confidence: 99%

Assembly of continuous high-resolution draft genome sequence ofHemicentrotus pulcherrimususing long-read sequencing

Komoto,

Ikeo,

Yaguchi

et al. 2023

Preprint

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The update of the draft genome assembly of sea urchin,Hemicentrotus pulcherrimus, which is widely studied in East Asia as a model organism of early development, was performed using Oxford nanopore long-read sequencing. The updated assembly provided ∼600 Mb genome sequences divided into 2,163 contigs with N50 = 516 kb. BUSCO completeness score and transcriptome model mapping ratio (TMMR) of the present assembly were obtained as 96.5 % and 77.8 % respectively. These results were more continuous with higher resolution than those by the previous version ofH. pulcerrimusdraft genome, HpulGenome_v1, where the number of scaffolds = 16,251 with a total of ∼100 Mb gaps, N50 = 143 kb, BUSCO completeness score = 86.1 %, and TMMR = 40.61. The obtained genome contained 36,055 gene models that were consistent with those in other echinoderms. Additionally, two tandem repeat sequences of early histone gene locus containing 47 copies and 34 copies of all histone genes, and 185 of the homologous sequences of the interspecifically conserved region of theArsinsulator, ArsInsC, were obtained. These results provide further advance for genome-wide research of development, gene regulation, and intranuclear structural dynamics of multicellular organisms usingHemicentrotus pulcherrimus.

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Unravelling the main immune repertoire of Paracentrotus lividus following Vibrio anguillarum bath challenge

Fernández-Boo,

Machado,

Castro

et al. 2024

Fish & Shellfish Immunology

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Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes

Cited by 28 publications

References 119 publications

Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

Assembly of continuous high-resolution draft genome sequence ofHemicentrotus pulcherrimususing long-read sequencing

Unravelling the main immune repertoire of Paracentrotus lividus following Vibrio anguillarum bath challenge

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