BackgroundThe ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.ResultsIn order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.ConclusionsThis work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

A hallmark of meiosis is chromosomal pairing, which requires telomere tethering and rotation on the nuclear envelope via microtubules, driving chromosome homology searches. Telomere pulling toward the centrosome forms the “zygotene chromosomal bouquet”. Here, we identified the “zygotene cilium” in oocytes. This cilium provides a cable system for the bouquet machinery, extending throughout the germline cyst. Using zebrafish mutants and live manipulations, we demonstrate that the cilium anchors the centrosome to counterbalance telomere pulling. The cilium is essential for bouquet and synaptonemal complex formation, oogenesis, ovarian development, and fertility. Thus, a cilium represents a conserved player in zebrafish and mouse meiosis, which sheds light on reproductive aspects in ciliopathies, and suggests that cilia can control chromosomal dynamics.

Oogenesis produces functional eggs and is essential for fertility, embryonic development, and reproduction. The zebrafish ovary is an excellent model to study oogenesis in vertebrates, and recent studies have identified multiple regulators in oocyte development through forward genetic screens, as well as reverse genetics by CRISPR mutagenesis. However, many developmental steps in oogenesis, in zebrafish and other species, remain poorly understood, and their underlying mechanisms are unknown. Here, we take a genomic approach to systematically uncover biological activities throughout oogenesis. We performed transcriptomic analysis on five stages of oogenesis, from the onset of oocyte differentiation through Stage III, which precedes oocyte maturation. These transcriptomes revealed thousands of differentially expressed genes across stages of oogenesis. We analyzed trends of gene expression dynamics along oogenesis, as well as their expression in pair-wise comparisons between stages. We determined their functionally enriched terms, identifying uniquely characteristic biological activities in each stage. These data identified two prominent developmental phases in oocyte differentiation and traced the accumulation of maternally deposited embryonic regulator transcripts in the developing oocyte. Our analysis provides the first molecular description for oogenesis in zebrafish, which we deposit online as a resource for the community. Further, the presence of multiple gene paralogs in zebrafish, and the exclusive curation by many bioinformatic tools of the single paralogs present in humans, challenge zebrafish genomic analyses. We offer an approach for converting zebrafish gene name nomenclature to the human nomenclature for supporting genomic analyses generally in zebrafish. Altogether, our work provides a valuable resource as a first step to uncover oogenesis mechanisms and candidate regulators and track accumulating transcripts of maternal regulators of embryonic development.

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Meiosis is a cellular program essential for the production of haploid gametes. A hallmark of meiosis is chromosomal pairing via synaptonemal complexes, and a major focus traditionally has been to understand synaptonemal complex formation. However, chromosomal pairing also depends on cytoplasmic counterparts that tether and rotate telomeres on the nuclear envelope, shuffling chromosomes and mechanically driving their homology searches. Rotating telomeres slide on perinuclear microtubules and are ultimately pulled towards the centrosome, forming a configuration called the zygotene chromosomal bouquet. The bouquet is universally conserved and is essential for pairing and fertility. However, despite its discovery in 1900, how the cytoplasmic counterparts of bouquet formation are mechanically regulated has remained enigmatic. Here, by studying zebrafish oogenesis, we report and comprehensively characterize a previously unrecognized cilium in oocytes, which we term the zygotene cilium. We show that the zygotene cilium specifically connects to the bouquet centrosome and constitutes a cable system of the cytoplasmic bouquet machinery. Farther, zygotene cilia extend throughout the germline cyst, a conserved cellular organization of germ cells. By analyzing multiple ciliary mutants, we demonstrate that the zygotene cilium is essential for chromosomal pairing, germ cell morphogenesis, ovarian development and fertility. We further show that the zygotene cilium is conserved in both male meiosis in zebrafish, as well as in mammalian oogenesis. Our work uncovers the novel concept of a cilium as a critical player in meiosis and sheds new light on reproduction phenotypes in ciliopathies. Furthermore, most cells in metazoans are ciliated and exhibit specific nuclear dynamics. We propose a cellular paradigm that cilia can control chromosomal dynamics.