Germ-soma differentiation is a hallmark of complex multicellular organisms, yet its origins are not well understood.
is a simple multicellular green alga that has recently evolved a simple germ-soma ...dichotomy with only two cell-types: large germ cells called gonidia and small terminally differentiated somatic cells. Here, we provide a comprehensive characterization of the gonidial and somatic transcriptomes of
to uncover fundamental differences between the molecular and metabolic programming of these cell-types. We found extensive transcriptome differentiation between cell-types, with somatic cells expressing a more specialized program overrepresented in younger, lineage-specific genes, and gonidial cells expressing a more generalist program overrepresented in more ancient genes that shared striking overlap with stem cell-specific genes from animals and land plants. Directed analyses of different pathways revealed a strong dichotomy between cell-types with gonidial cells expressing growth-related genes and somatic cells expressing an altruistic metabolic program geared toward the assembly of flagella, which support organismal motility, and the conversion of storage carbon to sugars, which act as donors for production of extracellular matrix (ECM) glycoproteins whose secretion enables massive organismal expansion.
orthologs of diurnally controlled genes from
a single-celled relative, were analyzed for cell-type distribution and found to be strongly partitioned, with expression of dark-phase genes overrepresented in somatic cells and light-phase genes overrepresented in gonidial cells- a result that is consistent with cell-type programs in
arising by cooption of temporal regulons in a unicellular ancestor. Together, our findings reveal fundamental molecular, metabolic, and evolutionary mechanisms that underlie the origins of germ-soma differentiation in
and provide a template for understanding the acquisition of germ-soma differentiation in other multicellular lineages.
Patterning of a multicellular body plan involves a coordinated set of developmental processes that includes cell division, morphogenesis, and cellular differentiation. These processes have been most ...intensively studied in animals and land plants; however, deep insight can also be gained by studying development in simpler multicellular organisms. The multicellular green alga Volvox carteri (Volvox) is an excellent model for the investigation of developmental mechanisms and their evolutionary origins. Volvox has a streamlined body plan that contains only a few thousand cells and two distinct cell types: reproductive germ cells and terminally differentiated somatic cells. Patterning of the Volvox body plan is achieved through a stereotyped developmental program that includes embryonic cleavage with asymmetric cell division, morphogenesis, and cell-type differentiation. In this review we provide an overview of how these three developmental processes give rise to the adult form in Volvox and how developmental mutants have provided insights into the mechanisms behind these events. We highlight the accessibility and tractability of Volvox and its relatives that provide a unique opportunity for studying development.
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•Volvox is a simple tractable model for investigating fundamental developmental questions.•Patterned symmetric and asymmetric embryonic cell divisions underlie cell fate specification.•Differences in postembryonic cell size dictate differentiation as germ or soma.•Cell shape changes drive inversion, a morphogenetic process analogous to animal gastrulation.•New technologies will enhance Volvox and its relatives as a model for evolution and development.
Abstract
Summary
ProteinPaint BAM track (ppBAM) is designed to assist variant review for cancer research and clinical genomics. With performant server-side computing and rendering, ppBAM supports ...on-the-fly variant genotyping of thousands of reads using Smith–Waterman alignment. To better visualize support for complex variants, reads are realigned against the mutated reference sequence using ClustalO. ppBAM also supports the BAM slicing API of the NCI Genomic Data Commons (GDC) portal, letting researchers conveniently examine genomic details of vast amounts of cancer sequencing data and reinterpret variant calls.
Availability and implementation
BAM track examples, tutorial, and GDC file access links are available at https://proteinpaint.stjude.org/bam/. Source code is available at https://github.com/stjude/proteinpaint.
The development of complex multicellular body plans relies on the differentiation of distinct cell types. These cell types establish the foundation for the construction of elaborate tissue and organ ...systems that create structural and functional complexity. Cell-type differentiation has evolved repeatedly across multicellular lineages; however, the evolutionary origins of this innovation are not well understood. Volvox carteri is a simple multicellular green alga that has recently evolved a simple division of labor between two cell types: germ cells called gonidia and terminally differentiated somatic cells. In this dissertation, I use two complementary approaches to characterize the gene regulatory networks controlling cell-type differentiation in Volvox. I then compare these networks to orthologous gene regulatory networks in the single-celled relative Chlamydomonas reinhardtii to interrogate the evolutionary origins of the cell-type differentiation program in this green algal lineage.In the first approach, I conducted a comprehensive transcriptomic analysis of the gonidial and somatic cell types of Volvox. Over 40% of Volvox genes were found to be expressed in a cell-type-regulated manner. Somatic cells expressed a more specialized genetic program overrepresented in younger, lineage-specific genes, while gonidial cells expressed a more generalist genetic program overrepresented in more ancient genes. Directed analyses of metabolic pathways revealed that gonidial cells preferentially express genes involved in carbon storage accumulation and cell growth, whereas somatic cells express an altruistic metabolic program geared towards the assembly of flagella and the biosynthesis and secretion of extracellular matrix material. Strikingly, I discovered a strong relationship between cell-type gene expression in Volvox and diurnal gene expression in the single-celled relative Chlamydomonas reinhardtii. Volvox orthologs of Chlamydomonas light-phase genes were preferentially expressed in gonidial cells, whereas Volvox orthologs of Chlamydomonas dark-phase genes were preferentially expressed in somatic cells—a result that is consistent with cell-type programs in Volvox arising by co-option of temporal/environmental regulons in a unicellular ancestor. Together, my findings reveal fundamental molecular, metabolic, and evolutionary mechanisms that underlie the origins of cell-type differentiation in Volvox and provide a template for understanding the acquisition of cell-type differentiation in other multicellular lineages.In the second approach, I began to characterize the gene regulatory network under the control of the RegA transcription factor. Maintenance of the somatic cell fate in Volvox is controlled by the regA locus, such that regA- somatic cells will dedifferentiate and redifferentiate as reproductive gonidial cells. The regA gene encodes a putative transcription factor that contains a conserved VARL domain, which harbors a SAND DNA-binding domain. I used DNA affinity purification sequencing (DAP-seq) to identify the candidate genomic binding sites of the RegA VARL domain. The VARL domain bound >1,000 candidate sites across the Volvox genome. Genes neighboring candidate VARL binding sites were enriched for somatic-specific genes. The VARL domain preferentially bound the DNA sequence TTCGA, which is similar to the DNA-binding motifs of SAND domain proteins in other species. The VARL binding motif was enriched near the transcription start sites of somatic-specific genes, suggesting the possibility that RegA functions as an activator of somatic-specific gene expression rather than as a repressor of gonidial-specific gene expression. This work has yielded insights into the DNA-binding properties of RegA and how RegA controls the gene regulatory network underlying somatic cell differentiation in Volvox. Taken together, the findings of this dissertation expand our understanding of the gene regulatory network underlying cell-type differentiation in Volvox and shed light on how this network evolved during the transition from unicellular to multicellular organisms.
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