BUSCADOR RECOLECTA

The emergence of new structures can often be linked to the evolution of novel
cell types that follows the rewiring of developmental gene regulatory subnetworks. Vertebrates are characterized by a complex body plan compared to
the other chordate clades and the question remains of whether and how the
emergence of vertebrate morphological innovations can be related to the
appearance of new embryonic cell populations. We previously proposed, by
studying mesoderm development in the cephalochordate amphioxus, a scenario for the evolution of the vertebrate head mesoderm. To further test this
scenario at the cell population level, we used scRNA-seq to construct a cell
atlas of the amphioxus neurula, stage at which the main mesodermal compartments are specified. Our data allowed us to validate the presence of a
prechordal-plate like territory in amphioxus. Additionally, the transcriptomic
profile of somite cell populations supports the homology between specific
territories of amphioxus somites and vertebrate cranial/pharyngeal and lateral
plate mesoderm. Finally, our work provides evidence that the appearance of
the specific mesodermal structures of the vertebrate head was associated to
both segregation of pre-existing cell populations, and co-option of new genes
for the control of myogenesis., The laboratory of H.E. and S.B. was supported by the CNRS, and by the “Agence Nationale de la Recheche” under the grants ANR-19-CE13-0011 to H.E. and ANR-21-CE13-0034 to S.B. Research in A.S-P. group was supported by the European Research Council (ERC-StG 851647 to A.S-P.) and the Spanish Ministry of Science and Innovation (PID2021-124757NB-I00 to A.S-P.). X.G-B. is supported by the European Union’s H2020 research and innovation program under Marie Sklodowska-Curie grant agreement 101031767 to X.G-B. A.E. was supported by FPI PhD fellowships from the Spanish Ministry of Science and Innovation. J.J.T. was supported by the Spanish Ministerio de Economía y Competitividad (grant PID2019-103921GB-I00 and PID2022-141288NB-I00 to J.T.). M.I. laboratory research has been funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (ERCCoG-LS2-101002275 to M.I.), by the Spanish Ministry of Economy and Competitiveness (PID2020-115040GB-I00 to M.I.) and by the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208 to M. I.)., Peer reviewed

Spermatogenesis is the biological process by which male sperm cells (spermatozoa) are produced in the testes. Beyond facilitating the transmission of genetic information, spermatogenesis also provides a potential framework for inter- and transgenerational inheritance of gene-regulatory states. While extensively studied in mammals, our understanding of spermatogenesis in anamniotes remains limited. Here we present a comprehensive single-cell multiomics resource, combining single-cell RNA sequencing (scRNA-seq) and single-cell chromatin accessibility (scATAC-seq) profiling, with base-resolution DNA methylome (WGBS) analysis of sorted germ cell populations from zebrafish (Danio rerio) testes. We identify the major germ cell types involved in zebrafish spermatogenesis as well as key drivers associated with these transcriptional states. Moreover, we describe localised DNA methylation changes associated with spermatocyte populations, as well as local and global changes in chromatin accessibility leading to chromatin compaction in spermatids. Notably, we identify loci that evade global chromatin compaction, and which remain accessible, suggesting a potential mechanism for the intergenerational transmission of gene-regulatory states. In summary, this high-resolution atlas of zebrafish spermatogenesis provides a valuable resource for studying vertebrate germ cell development and epigenetic inheritance, while offering a robust framework for comparative analyses across diverse models of germ cell biology.