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Tiozzo, S.

Publications and source records attributed to Tiozzo, S..

7 recordsLinked to original sources

Multi-stage single-cell atlas of Botryllus schlosseri asexual development unveils dedifferentiating bud founder cells

Colonial tunicates are the only chordates capable of forming fully functional bodies from somatic tissues through non-embryonic development, known as budding. In Botryllus schlosseri, this agametic process, termed peribranchial budding, generates new zooids in a stereotyped, cyclical manner from a cluster of cells within the peribranchial epithelium. Despite detailed morphological characterization, the molecular and cellular underpinnings of budding initiation remain poorly understood. Here, we present the first single-cell transcriptomic atlas of B. schlosseri peribranchial budding, encompassing multiple stages from pre-budding to near-mature zooid. This high-resolution atlas captures the diversity of cell types involved in budding and their dynamics enabling precise cluster annotation and lineage trajectory inference. While circulating mesenchymal cells exhibit transcriptional hallmarks of stem-like states, we found no definitive evidence of broad contribution to bud onset and early morphogenesis beyond hematopoietic and gonadal lineages. Instead, we identified a distinct founder cell population arising from peribranchial epithelium, marked by a unique transcriptional profile and progressive acquisition of developmental potency. This supports a model in which budding is initiated by dedifferentiation of committed epithelial cells rather than activation of multi- or pluripotent stem cells. Furthermore, we highlight signaling pathways, including GNRHR-like receptors, that may couple metabolic state with developmental progression. Altogether, our data suggest that peribranchial budding in B. schlosseri is driven by potential reprogramming within epithelial tissues. This work provides a foundational resource for studying non-embryonic development and the evolution of regenerative strategies in chordates.

developmental biology↗

Genetic and functional diversity of allorecognition receptors in the urochordate, Botryllus schlosseri

Allorecognition in Botryllus schlosseri is controlled by a highly polymorphic locus (the fuhc), and functionally similar to missing-self recognition utilized by Natural Killer cells-compatibility is determined by sharing a self-allele, and integration of activating and inhibitory signals determines outcome. We had found these signals were generated by two fuhc-encoded receptors, called fester and uncle fester. Here we show that fester genes are members of an extended family consisting of >37 loci, and co-expressed with an even more diverse gene family-the fester co-receptors (FcoR). The FcoRs are membrane proteins related to fester, but include conserved tyrosine motifs, including ITIMs and hemITAMs. Both genes are encoded in highly polymorphic haplotypes on multiple chromosomes, revealing an unparalleled level of diversity of innate receptors. Our results also suggest that ITAM/ITIM signal integration is a deeply conserved mechanism that has allowed convergent evolution of innate and adaptive cell-based recognition systems.

immunology↗

First chromosome-level genome assembly of the colonial tunicate Botryllus schlosseri

Botryllus schlosseri (Tunicata) is a colonial chordate that has long been studied for its multiple developmental pathways and regenerative abilities and its genetically determined allorecognition system based on a polymorphic locus that controls chimerism and cell parasitism. We present the first chromosome-level genome assembly from an isogenic colony of B. schlosseri clade A1 using a mix of long and short reads scaf-folded using Hi-C. This haploid assembly spans 533 Mb, of which 96% are found in 16 chromosome-scale scaffolds. With a BUSCO completeness of 91.2%, this complete and contiguous B. schlosseri genome assembly provides a valuable genomic resource for the scientific community and lays the foundation for future investigations into the molecular mechanisms underlying coloniality, regeneration, histocompatibility, and the immune system in tunicates.

genomics↗

Comparing dormancy in two distantly related tunicates reveals morphological, molecular, and ecological convergences and repeated co-option

Many asexually-propagating marine invertebrates can survive extreme environmental conditions by developing dormant structures, i.e., morphologically simplified bodies that retain the capacity to completely regenerate a functional adult when conditions return to normal. Here, we examine the environmental, morphological, and molecular characteristics of dormancy in two distantly related clonal tunicate species: Polyandrocarpa zorritensis and Clavelina lepadiformis. In both species, we report that the dormant structures are able to withstand harsher temperature and salinity conditions compared to the adult, and are the dominant forms these species employ to survive the colder winter months. By finely controlling the entry and exit of dormancy in laboratory-reared individuals, we were able to select and characterize the morphology of dormant structures associated with their transcriptome dynamics. In both species, we identified putative stem and nutritive cells in structures that resemble the earliest stages of asexual propagation. By characterizing gene expression during dormancy and regeneration into the adult body plan (i.e., germination), we observed that genes which control dormancy and environmental sensing in other metazoans, notably HIF- and insulin signaling genes, are also expressed in tunicate dormancy. Germination-related genes in these two species, such as the retinoic acid pathway, are also found in other unrelated clonal tunicates during asexual development. These results are suggestive of repeated exaptation of conserved eco-physiological and regeneration programs for the origin of novel dormancy-germination processes across distantly related animal taxa.

developmental biology↗

The onset of whole-body regeneration in Botryllus schlosseri: morphological and molecular characterization

Colonial tunicates are the only chordates that regularly regenerate a fully functional whole body as part of their asexual life cycle, starting from specific epithelia and/or mesenchymal cells. In addition, in some species, whole-body regeneration (WBR) can also be triggered by extensive injuries, which deplete most of their tissues and organs and leave behind only small fragments of their body. In this manuscript, we characterized the onset of WBR in Botryllus schlosseri, one colonial tunicate long used as a laboratory model. We first analyzed the transcriptomic response to a WBR-triggering injury. Then, through morphological characterization, in vivo observations via time-lapse, vital dyes, and cell transplant assays, we started to reconstruct the dynamics of the cells triggering regeneration, highlighting an interplay between mesenchymal and epithelial cells. The dynamics described here suggest that WBR in B. schlosseri is initiated by extravascular tissue fragments derived from the injured individuals rather than particular populations of blood-borne cells, as has been described in closely related species. The morphological and molecular datasets here reported provide the background for future mechanistic studies of the WBR ontogenesis in B. schlosseri and allow to compare it with other regenerative processes occurring in other tunicate species and possibly independently evolved.

developmental biology↗

Colonial ascidians strongly preyed upon, yet dominate the substrate in a subtropical fouling community

Higher diversity and dominance at lower latitudes has been suggested for colonial species. We verified the latitudinal pattern in species richness of ascidians, finding that higher colonial-to-solitary species ratios occur in the tropics and subtropics. At the latitudinal region with the highest ratio, in south-eastern Brazil, we confirmed that colonial species dominate the space on artificial plates in two independent studies of five fouling communities. We manipulated settlement plates to measure effects of predation and competition on growth and survivorship of colonial vs. solitary ascidians. Eight ascidian species were subjected to a predation treatment, i.e. caged vs. exposed to predators, and a competition treatment, i.e. leaving vs. removing competitors, to assess main and interactive effects. Predation had a greater effect on growth and survivorship of colonial compared to solitary species, whereas competition did not show consistent patterns between the two life histories. We hypothesize that colonial ascidians dominate at this subtropical site despite being highly preyed upon because they regrow when partially consumed and can adjust in shape and space to grow into refuges. We contend that these means of avoiding mortality from predation can have large influences on the diversification patterns of colonial species at low latitudes, where predation intensity is greater.

ecology↗

Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis

BackgroundIn chordates cardiac and body muscles arise from different embryonic origins. Myogenesis can in addition be triggered in adult organisms, during asexual development or regeneration. In the non-vertebrate ascidians, muscles originate from embryonic precursors regulated by a conserved set of genes that orchestrate cell behavior and dynamics during development. In colonial ascidians, besides embryogenesis and metamorphosis, an adult can propagate asexually via blastogenesis, skipping embryo and larval stages, and form anew the adult body, including the complete body musculature.\n\nResultsTo investigate the cellular origin and mechanisms that trigger non-embryonic myogenesis, we followed the expression of ascidian myogenic genes during Botryllus schlosseri blastogenesis, and reconstructed the dynamics of muscle precursors. Based on the expression dynamics of Tbx1/10, Ebf, Mrf, Myh3 for body wall and of FoxF, Tbx1/10, Nk4, Myh2 for heart development we show that the embryonic factors regulating myogenesis are only partially co-opted in blastogenesis, and propose that the cellular precursors contributing to heart or body muscles have different origins.\n\nConclusionsRegardless of the developmental pathway, non-embryonic myogenesis shares a similar molecular and anatomical setup as embryonic myogenesis, but implements co-option and loss of molecular modules.

developmental biology↗