Biology subjects

Bump, P.

Publications and source records attributed to Bump, P..

7 recordsLinked to original sources

bioRxiv2025

Major cell type differences between larval and adult hemichordate body plans

A major gap in our understanding of animal development is how adult body plans arise in animals with indirect development, where adults emerge from the transformation of a distinct larval form during metamorphosis. We address this question by examining cellular changes in the enteropneust hemichordate Schizocardium californicum, a species with a complex lifecycle and dramatic metamorphosis. Employing whole-body single-cell RNA sequencing, we chart the cellular composition and transcriptional dynamics of larval, metamorphosis, and adult stages. Our tissue level atlas reveals that ectodermal and endodermal cell types in larvae and adults occupy distinct transcriptional spaces, showing greater similarity to other cell types within the same life stage than to their counterparts in the opposite stage. In contrast, mesodermal cell types from both larvae and adults cluster closely together, indicating conserved transcriptional profiles. These findings demonstrate that the extensive morphological reorganization during metamorphosis is paralleled by profound shifts in cell-type specific transcriptional programs, highlighting the complexity of the larva-to-adult transition.

developmental biology↗

bioRxiv2023

Chromatin profiling data indicate regulatory mechanisms for differentiation during development in the acoel Hofstenia miamia

Chromatin profiling data can corroborate and generate hypotheses for regulatory events that underlie the control of gene expression in any biological process. Here, we applied the Assay for Transposase Accessible Chromatin (ATAC) sequencing to build a catalog of putative regulatory DNA during the process of embryonic development in an acoel. Acoels represent an enigmatic phylum-level lineage of animals, the Xenacoelomorpha, which is placed either as a sister-group to all other animals with bilateral symmetry or as an early-diverging ambulacrarian, two alternative phylogenetic placements that both position acoels equally well to inform the evolution of developmental mechanisms. We focused on the acoel Hofstenia miamia, a.k.a. the three-banded panther worm, which has emerged as a new laboratory research organism for whole-body regeneration that also enables the study of development from zygote to hatching. We profiled chromatin landscapes over a time course encompassing many major morphological events, including gastrulation, axial patterning, and differentiation of tissues such as epidermis and muscle. Broad patterns of chromatin accessibility and predicted binding of various transcription factor (TF) motifs identified major biological processes and their putative regulators, and we noted that differential accessibility tended to precede major developmental transitions in embryogenesis. Focused analysis of TF binding combined with single-cell RNA-seq data provided regulatory linkages for genes in a previously hypothesized differentiation trajectory for epidermis and generated new hypotheses for gene regulatory networks associated with the formation of muscle. This work provides a platform for the identification of developmental mechanisms in Hofstenia and enables comparisons of embryogenesis in acoels to other animals as well as comparisons of embryogenesis to regeneration.

developmental biology↗

bioRxiv2023

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

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 flava and Schizocardium 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.

evolutionary biology↗

bioRxiv2022

Peripheral and central employment of acid-sensing ion channels during early bilaterian evolution

Nervous systems are endowed with rapid chemosensation and intercellular signaling by ligand-gated ion channels (LGICs). While a complex, bilaterally symmetrical nervous system is a major innovation of bilaterian animals, the employment of specific LGICs during early bilaterian evolution is poorly understood. We therefore questioned bilaterian animals employment of acid-sensing ion channels (ASICs), LGICs that mediate fast excitatory responses to decreases in extracellular pH in vertebrate neurons. Our phylogenetic analysis identified an earlier emergence of ASICs from the overarching DEG/ENaC superfamily than previously thought and suggests that ASICs were a bilaterian innovation. Our broad examination of ASIC gene expression and biophysical function in each major bilaterian lineage of Xenacoelomorpha, Protostomia, and Deuterostomia, suggests that the earliest bilaterian ASICs were probably expressed in the periphery, before being incorporated into the brain as it emerged independently in certain deuterostomes and xenacoelomorphs. The loss of certain peripheral cells from Ecdysozoa when they split from other protostomes likely explains their loss of ASICs, and thus the absence of ASICs in model organisms Drosophila and C. elegans. Thus, our use of diverse bilaterians in the investigation of LGIC expression and function offers a unique hypothesis on the employment of LGICs in early bilaterian evolution.

evolutionary biology↗

bioRxiv2022

Comparisons of cell proliferation and cell death across life histories in the hemichordate Schizocardium californicum

BackgroundThere are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when the tissue that will give rise to the adult originates. Here we present patterns of cell proliferation and cell death during larval development, metamorphosis, and adult body plan formation, in the hemichordate Schizocardium californium to answer these questions. ResultsWe identified distinct patterns of cell proliferation between larval and adult body plan formation of S. californicum. We found that some adult tissues proliferate prior to the start of any morphological metamorphosis. Additionally, we describe a genetic signature of proliferative cells with an irradiation approach that revealed markers shared between the life history states and others that are unique to larvae or juveniles. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis. ConclusionsCell proliferation during the development of S. californicum has distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferate and give rise to the larva and juvenile have a genetic signature that is more suggestive of a heterogeneous pool of proliferative progenitors versus a population of pluripotent set-aside cells. Taken together, we propose that S. californicum has a transformative metamorphosis that may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.

developmental biology↗

bioRxiv2020

A single origin of animal excretory organs

Excretion is an essential physiological process, carried out by all living organisms regardless of their size or complexity(1-3). Most animals, which include both protostomes (e.g. flies, flatworms) and deuterostomes (e.g. humans, sea urchins) (together Nephrozoa(4, 5)), possess specialized excretory organs. Those organs exhibit an astonishing diversity, ranging from units composed of just three distinct cells (e.g. protonephridia) to complex structures, built by millions of cells of multiple types with divergent morphology and function (e.g. vertebrate kidneys)(6, 7). Although some molecular similarities between the development of kidneys of vertebrates and the regeneration of the protonephridia of flatworms have been reported(8, 9), the molecular development of nephrozoan excretory organs has never been systematically studied in a comparative context(6). Here we show that a set of highly conserved transcription factors and structural proteins is expressed during the development of excretory organs of six species that represent major protostome lineages and non-vertebrate deuterostomes. We demonstrate that the molecular similarity witnessed in the vertebrate kidney and flatworm protonephridia(8) is also seen in the developing excretory organs of other Nephrozoa. In addition, orthologous structural proteins forming the ultrafiltration apparatus are expressed in all these organs in the filter-forming cells. Our results strongly suggest that excretory organs are homologous and are patterned by the conserved set of developmental genes. We propose that the last common nephrozoan ancestor possessed an ultrafiltration-based, ciliated excretory organ, a structure that later gave rise to the vast diversity of extant excretory organs, including the human kidney. Significance statementMost of the bilaterally symmetrical animals excrete through specialized excretory organs, such as kidneys and nephridia. However, due to the morphological diversity of these organs, it remains unknown whether those structures evolved from a common ancestral organ or appeared several times independently during evolution. In order to answer the question about the origin of excretory organs we investigated the molecular pathways and structural genes involved in the development of nephridia in 6 animal species representing major evolutionary lineages. We show that diverse excretory organs share an ancient molecular patterning and structural molecules. Our results provide strong evidence that all excretory organs originated from a single, simple organ that performed urine production by ultrafiltration in deep geological past.

evolutionary biology↗

bioRxiv2017

Genome-Wide Analysis of Facial Regionalization in Zebrafish

Patterning of the facial skeleton involves the precise deployment of thousands of genes in distinct regions of the pharyngeal arches. Despite the significance for craniofacial development, how genetic programs drive this regionalization remains incompletely understood. Here we use combinatorial labeling of zebrafish cranial neural crest-derived cells (CNCCs) to define global gene expression along the dorsoventral axis of the developing arches. Intersection of region-specific transcriptomes with expression changes in response to signaling perturbations demonstrates complex roles for Endothelin1 (Edn1) signaling in the intermediate joint-forming region yet a surprisingly minor role in ventral-most regions. Analysis of co-variance across multiple sequencing experiments further reveals clusters of coregulated genes, with in situ hybridization confirming the domain-specific expression of novel genes. We then performed mutational analysis of a number of these genes, which uncovered antagonistic functions of two new Edn1 targets, follistatin a (fsta) and emx2, in regulating cartilaginous joints in the hyoid arch. Our unbiased discovery and functional analysis of genes with regional expression in zebrafish arch CNCCs reveals complex regulation by Ednl and points to novel candidates for craniofacial disorders.\n\nSummary StatementUsing zebrafish to purify distinct groups of embryonic cells, Askary et al. have created a detailed map of how thousands of genes are deployed to shape the developing face.

developmental biology↗