Mineralized Cartilage and Bone-Like Tissues in Chondrichthyans Offer Potential Insights Into the Evolution and Development of Mineralized Tissues in the Vertebrate Endoskeleton

The impregnation of biominerals into the extracellular matrix of living organisms, a process termed biomineralization, gives rise to diverse mineralized (or calcified) tissues in vertebrates. Preservation of mineralized tissues in the fossil record has provided insights into the evolutionary history of vertebrates and their skeletons. However, current understanding of the vertebrate skeleton and of the processes underlying its formation is biased towards biomedical models such as the tetrapods mouse and chick. Chondrichthyans (sharks, skates, rays, and chimaeras) and osteichthyans are the only vertebrate groups with extant (living) representatives that have a mineralized skeleton, but the basal phylogenetic position of chondrichthyans could potentially offer unique insights into skeletal evolution. For example, bone is a vertebrate novelty, but the internal supporting skeleton (endoskeleton) of extant chondrichthyans is commonly described as lacking bone. The molecular and developmental basis for this assertion is yet to be tested. Subperichondral tissues in the endoskeleton of some chondrichthyans display mineralization patterns and histological and molecular features of bone, thereby challenging the notion that extant chondrichthyans lack endoskeletal bone. Additionally, the chondrichthyan endoskeleton demonstrates some unique features and others that are potentially homologous with other vertebrates, including a polygonal mineralization pattern, a trabecular mineralization pattern, and an unconstricted perichordal sheath. Because of the basal phylogenetic position of chondrichthyans among all other extant vertebrates with a mineralized skeleton, developmental and molecular studies of chondrichthyans are critical to flesh out the evolution of vertebrate skeletal tissues, but only a handful of such studies have been carried out to date. This review discusses morphological and molecular features of chondrichthyan endoskeletal tissues and cell types, ultimately emphasizing how comparative embryology and transcriptomics can reveal homology of mineralized skeletal tissues (and their cell types) between chondrichthyans and other vertebrates.

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Developmental paleobiology of the vertebrate skeleton

Journal of Paleontology ◽

10.1666/13-107 ◽

2014 ◽

Vol 88 (4) ◽

pp. 676-683 ◽

Cited By ~ 8

Author(s):

Martin Rücklin ◽

Philip C. J. Donoghue ◽

John A. Cunningham ◽

Federica Marone ◽

Marco Stampanoni

Keyword(s):

Developmental Stages ◽

Growth Stages ◽

Developmental Evolution ◽

Non Invasive ◽

Mineralized Tissues ◽

Crucial Information ◽

Pros And Cons ◽

Living Organisms ◽

Third Dimension ◽

Vertebrate Skeleton

Studies of the development of organisms can reveal crucial information on homology of structures. Developmental data are not peculiar to living organisms, and they are routinely preserved in the mineralized tissues that comprise the vertebrate skeleton, allowing us to obtain direct insight into the developmental evolution of this most formative of vertebrate innovations. The pattern of developmental processes is recorded in fossils as successive stages inferred from the gross morphology of multiple specimens and, more reliably and routinely, through the ontogenetic stages of development seen in the skeletal histology of individuals. Traditional techniques are destructive and restricted to a 2-D plane with the third dimension inferred. Effective non-invasive methods of visualizing paleohistology to reconstruct developmental stages of the skeleton are necessary.In a brief survey of paleohistological techniques we discuss the pros and cons of these methods. The use of tomographic methods to reconstruct development of organs is exemplified by the study of the placoderm dentition. Testing evidence for the presence of teeth in placoderms, the first jawed vertebrates, we compare the methods that have been used. These include inferring development from morphology, and using serial sectioning, microCT or synchrotron X-ray tomographic microscopy (SRXTM), to reconstruct growth stages and directions of growth. The ensuing developmental interpretations are biased by the methods and degree of inference. The most direct and reliable method is using SRXTM data to trace sclerochronology. The resulting developmental data can be used to resolve homology and test hypotheses on the origin of evolutionary novelties.

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Cells at the Edge: The Dentin–Bone Interface in Zebrafish Teeth

Frontiers in Physiology ◽

10.3389/fphys.2021.723210 ◽

2021 ◽

Vol 12 ◽

Author(s):

Joana T. Rosa ◽

Paul Eckhard Witten ◽

Ann Huysseune

Keyword(s):

Calcium Binding ◽

Evolutionary History ◽

Cell Types ◽

Tissue Type ◽

Dentinal Tubule ◽

Jaw Bone ◽

Attachment Structures ◽

Mineralized Tissues ◽

History Of ◽

Bona Fide

Bone-producing osteoblasts and dentin-producing odontoblasts are closely related cell types, a result from their shared evolutionary history in the ancient dermal skeleton. In mammals, the two cell types can be distinguished based on histological characters and the cells’ position in the pulp cavity or in the tripartite periodontal complex. Different from mammals, teleost fish feature a broad diversity in tooth attachment modes, ranging from fibrous attachment to firm ankylosis to the underlying bone. The connection between dentin and jaw bone is often mediated by a collar of mineralized tissue, a part of the dental unit that has been termed “bone of attachment”. Its nature (bone, dentin, or an intermediate tissue type) is still debated. Likewise, there is a debate about the nature of the cells secreting this tissue: osteoblasts, odontoblasts, or yet another (intermediate) type of scleroblast. Here, we use expression of the P/Q rich secretory calcium-binding phosphoprotein 5 (scpp5) to characterize the cells lining the so-called bone of attachment in the zebrafish dentition. scpp5 is expressed in late cytodifferentiation stage odontoblasts but not in the cells depositing the “bone of attachment”. nor in bona fide osteoblasts lining the supporting pharyngeal jaw bone. Together with the presence of the osteoblast marker Zns-5, and the absence of covering epithelium, this links the cells depositing the “bone of attachment” to osteoblasts rather than to odontoblasts. The presence of dentinal tubule-like cell extensions and the near absence of osteocytes, nevertheless distinguishes the “bone of attachment” from true bone. These results suggest that the “bone of attachment” in zebrafish has characters intermediate between bone and dentin, and, as a tissue, is better termed “dentinous bone”. In other teleosts, the tissue may adopt different properties. The data furthermore support the view that these two tissues are part of a continuum of mineralized tissues. Expression of scpp5 can be a valuable tool to investigate how differentiation pathways diverge between osteoblasts and odontoblasts in teleost models and help resolving the evolutionary history of tooth attachment structures in actinopterygians.

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Regulation of Cell Fate Decisions in Early Mammalian Embryos

Annual Review of Animal Biosciences ◽

10.1146/annurev-animal-021419-083841 ◽

2020 ◽

Vol 8 (1) ◽

pp. 377-393

Author(s):

Ramiro Alberio

Keyword(s):

Cell Fate ◽

Regulatory Networks ◽

New Technologies ◽

Cell Types ◽

Cell Fate Decisions ◽

Evolution And Development ◽

Mammalian Embryos ◽

Adult Organism ◽

Gene Regulatory ◽

Comparative Embryology

Early embryogenesis is characterized by the segregation of cell lineages that fulfill critical roles in the establishment of pregnancy and development of the fetus. The formation of the blastocyst marks the emergence of extraembryonic precursors, needed for implantation, and of pluripotent cells, which differentiate toward the major lineages of the adult organism. The coordinated emergence of these cell types shows that these processes are broadly conserved in mammals. However, developmental heterochrony and changes in gene regulatory networks highlight unique evolutionary adaptations that may explain the diversity in placentation and in the mechanisms controlling pluripotency in mammals. The incorporation of new technologies, including single-cell omics, imaging, and gene editing, is instrumental for comparative embryology. Broadening the knowledge of mammalian embryology will provide new insights into the mechanisms driving evolution and development. This knowledge can be readily translated into biomedical and biotechnological applications in humans and livestock, respectively.

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Filling the Gaps in the Cyanobacterial Tree of Life—Metagenome Analysis of Stigonema ocellatum DSM 106950, Chlorogloea purpurea SAG 13.99 and Gomphosphaeria aponina DSM 107014

Genes ◽

10.3390/genes12030389 ◽

2021 ◽

Vol 12 (3) ◽

pp. 389

Author(s):

Pia Marter ◽

Sixing Huang ◽

Henner Brinkmann ◽

Silke Pradella ◽

Michael Jarek ◽

...

Keyword(s):

Heterotrophic Bacteria ◽

Morphological Diversity ◽

Cell Types ◽

Phylogenetic Position ◽

Metagenome Analysis ◽

New Family ◽

Metagenome Sequencing ◽

Axenic Strains ◽

Reliable Classification ◽

Metagenomic Assembly

Cyanobacteria represent one of the most important and diverse lineages of prokaryotes with an unparalleled morphological diversity ranging from unicellular cocci and characteristic colony-formers to multicellular filamentous strains with different cell types. Sequencing of more than 1200 available reference genomes was mainly driven by their ecological relevance (Prochlorococcus, Synechococcus), toxicity (Microcystis) and the availability of axenic strains. In the current study three slowly growing non-axenic cyanobacteria with a distant phylogenetic positioning were selected for metagenome sequencing in order to (i) investigate their genomes and to (ii) uncover the diversity of associated heterotrophs. High-throughput Illumina sequencing, metagenomic assembly and binning allowed us to establish nearly complete high-quality draft genomes of all three cyanobacteria and to determine their phylogenetic position. The cyanosphere of the limnic isolates comprises up to 40 heterotrophic bacteria that likely coexisted for several decades, and it is dominated by Alphaproteobacteria and Bacteriodetes. The diagnostic marker protein RpoB ensured in combination with our novel taxonomic assessment via BLASTN-dependent text-mining a reliable classification of the metagenome assembled genomes (MAGs). The detection of one new family and more than a dozen genera of uncultivated heterotrophic bacteria illustrates that non-axenic cyanobacteria are treasure troves of hidden microbial diversity.

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Clinical, Pathological and Molecular Characteristics of Chilean Patients with Early-, Intermediate- and Late-Onset Colorectal Cancer

Cells ◽

10.3390/cells10030631 ◽

2021 ◽

Vol 10 (3) ◽

pp. 631

Author(s):

Karin Alvarez ◽

Alessandra Cassana ◽

Marjorie De La Fuente ◽

Tamara Canales ◽

Mario Abedrapo ◽

...

Keyword(s):

Colorectal Cancer ◽

Family History ◽

Age Of Onset ◽

Late Onset ◽

Molecular Characteristics ◽

Family History Of Cancer ◽

Molecular Features ◽

Age Of Diagnosis ◽

History Of ◽

History Of Cancer

Colorectal cancer (CRC) is the second most frequent neoplasm in Chile and its mortality rate is rising in all ages. However, studies characterizing CRC according to the age of onset are still lacking. This study aimed to identify clinical, pathological, and molecular features of CRC in Chilean patients according to the age of diagnosis: early- (≤50 years; EOCRC), intermediate- (51–69 years; IOCRC), and late-onset (≥70 years; LOCRC). The study included 426 CRC patients from Clinica Las Condes, between 2007 and 2019. A chi-square test was applied to explore associations between age of onset and clinicopathological characteristics. Body Mass Index (BMI) differences according to age of diagnosis was evaluated through t-test. Overall (OS) and cancer-specific survival (CSS) were estimated by the Kaplan–Meier method. We found significant differences between the age of onset, and gender, BMI, family history of cancer, TNM Classification of Malignant Tumors stage, OS, and CSS. EOCRC category was characterized by a family history of cancer, left-sided tumors with a more advanced stage of the disease but better survival at 10 years, and lower microsatellite instability (MSI), with predominant germline mutations. IOCRC has shown clinical similarities with the EOCRC and molecular similarities to the LOCRC, which agrees with other reports.

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Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts

Genome Biology and Evolution ◽

10.1093/gbe/evz155 ◽

2019 ◽

Cited By ~ 4

Author(s):

Sergio A Muñoz-Gómez ◽

Keira Durnin ◽

Laura Eme ◽

Christopher Paight ◽

Christopher E Lane ◽

...

Keyword(s):

Life Style ◽

Metabolic Pathways ◽

Evolutionary History ◽

Phylogenetic Analyses ◽

Phylogenetic Position ◽

Biosynthetic Pathways ◽

History Of ◽

Sea Squirts ◽

Shed Light ◽

Apicoplast Genome

Abstract A most interesting exception within the parasitic Apicomplexa is Nephromyces, an extracellular, probably mutualistic, endosymbiont found living inside molgulid ascidian tunicates (i.e., sea squirts). Even though Nephromyces is now known to be an apicomplexan, many other questions about its nature remain unanswered. To gain further insights into the biology and evolutionary history of this unusual apicomplexan, we aimed to (1) find the precise phylogenetic position of Nephromyces within the Apicomplexa, (2) search for the apicoplast genome of Nephromyces, and (3) infer the major metabolic pathways in the apicoplast of Nephromyces. To do this, we sequenced a metagenome and a metatranscriptome from the molgulid renal sac, the specialized habitat where Nephromyces thrives. Our phylogenetic analyses of conserved nucleus-encoded genes robustly suggest that Nephromyces is a novel lineage sister to the Hematozoa, which comprises both the Haemosporidia (e.g., Plasmodium) and the Piroplasmida (e.g., Babesia and Theileria). Furthermore, a survey of the renal sac metagenome revealed 13 small contigs that closely resemble the genomes of the non-photosynthetic reduced plastids, or apicoplasts, of other apicomplexans. We show that these apicoplast genomes correspond to a diverse set of most closely related but genetically divergent Nephromyces lineages that co-inhabit a single tunicate host. In addition, the apicoplast of Nephromyces appears to have retained all biosynthetic pathways inferred to have been ancestral to parasitic apicomplexans. Our results shed light on the evolutionary history of the only probably mutualistic apicomplexan known, Nephromyces, and provide context for a better understanding of its life style and intricate symbiosis.

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Phylogenetic position and evolutionary history of the turtle and whale barnacles (Cirripedia: Balanomorpha: Coronuloidea)

Molecular Phylogenetics and Evolution ◽

10.1016/j.ympev.2012.12.018 ◽

2013 ◽

Vol 67 (1) ◽

pp. 9-14 ◽

Cited By ~ 16

Author(s):

Ryota Hayashi ◽

Benny K.K. Chan ◽

Noa Simon-Blecher ◽

Hiromi Watanabe ◽

Tamar Guy-Haim ◽

...

Keyword(s):

Evolutionary History ◽

Phylogenetic Position ◽

History Of

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Notes on the generic position of Brassica deserti (Brassicaceae)

Israel Journal of Plant Sciences ◽

10.1163/22238980-20191087 ◽

2019 ◽

Vol 66 (1-2) ◽

pp. 89-93

Author(s):

Jotham Ziffer-Berger ◽

Alexandra Keren-Keiserman ◽

Adi Doron-Faigenboim ◽

Klaus Mummenhoff ◽

Oz Barazani

Keyword(s):

Mediterranean Area ◽

Morphological Data ◽

Phylogenetic Position ◽

Molecular Tools ◽

East Mediterranean ◽

Phylogenetic Groups ◽

5.8S Rdna ◽

The Core ◽

Generic Position ◽

History Of

Molecular tools provide new insights into phylogenetic relationships of plant species, and by relating phylogenetic groups to their geographical distribution, we can cast light upon the evolution history of plant clades. In the current study, we evaluated the phylogenetic position of the Sinai endemic Brassica deserti (Brassicaceae), later renamed as Erucastrum deserti, based on morphological data and 5.8S rDNA and ITS (Internal Transcribed Spacer) regions. Our results indicate that B. deserti belongs to an East-Mediterranean – Saharo Arabian clade and was not assigned to the core Brassica and Erucastrum clades, respectively, which evolved in the West Mediterranean area. We tentatively conclude that Brassica deserti evolved independently of core Brassica and Erucastrum.

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Natural history of ABC systems: not only transporters

Essays in Biochemistry ◽

10.1042/bse0500019 ◽

2011 ◽

Vol 50 ◽

pp. 19-42 ◽

Cited By ~ 20

Author(s):

Elie Dassa

Keyword(s):

Common Ancestor ◽

Three Dimensional ◽

Last Common Ancestor ◽

Abc Proteins ◽

Hypothetical Scenario ◽

History Of ◽

Phylogenetic Perspective ◽

Living Organisms

In recent years, our understanding of the functioning of ABC (ATP-binding cassette) systems has been boosted by the combination of biochemical and structural approaches. However, the origin and the distribution of ABC proteins among living organisms are difficult to understand in a phylogenetic perspective, because it is hard to discriminate orthology and paralogy, due to the existence of horizontal gene transfer. In this chapter, I present an update of the classification of ABC systems and discuss a hypothetical scenario of their evolution. The hypothetical presence of ABC ATPases in the last common ancestor of modern organisms is discussed, as well as the additional possibility that ABC systems might have been transmitted to eukaryotes, after the two endosymbiosis events that led to the constitution of eukaryotic organelles. I update the functional information of selected ABC systems and introduce new families of ABC proteins that have been included recently into this vast superfamily, thanks to the availability of high-resolution three-dimensional structures.

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Three new Cenomanian conifers from El Chango (Chiapas, Mexico) offer a snapshot of the geographic mosaic of the Mesozoic conifer decline

10.1101/2021.09.01.458614 ◽

2021 ◽

Author(s):

Ixchel Gonzalez-Ramirez ◽

Sergio RS Cevallos-Ferriz ◽

Carl Rothfels

Keyword(s):

Evolutionary History ◽

Mixed Forest ◽

Freshwater Ecosystems ◽

Total Evidence ◽

Morphological Data ◽

Phylogenetic Position ◽

Dominant Group ◽

Geographic Mosaic ◽

History Of ◽

Rare Opportunity

Premise of study: El Chango is a recently discovered quarry that contains extremely well preserved fossils. The Cenomanian age of the locality corresponds to a time when the global flora was transitioning from gymnosperm- to angiosperm-dominated, yet conifers predominate in this locality. These fossils thus provide a rare opportunity to understand the replacement of conifers by angiosperms as the dominant group of plants. Methods: We collected material from El Chango in annual expeditions (2010 to 2014). We selected the three most abundant and best preserved conifer morphotypes and conducted a total-evidence (i.e., including molecular and morphological data) phylogenetic analysis of a sample of 72 extant conifer species plus the three fossils. We use these results to inform our taxonomic decisions. Results: We obtained four equally most-parsimonious trees (consistency index = 44.1%, retention index = 78.8%). Despite ambiguous relationships among some extant taxa, the three fossil conifers had the same phylogenetic position in all four most parsimonious trees; we describe these species as new: Sequoiadendron helicalancifolium sp. nov. (Cupressaceae), and Microcachrys rhomboidea sp. nov. and Dacrydium bifoliosus sp. nov (Podocarpaceae). The ecosystem is interpreted as a coastal humid mixed forest. Conclusions: Our findings contribute to the understanding of Cenomanian equatorialregions, and support the hypothesis of a geographically and ecologically structured rise of angiosperms, with conifers remaining dominant in brackish-water and angiosperms becoming dominant in freshwater-ecosystems. These fossils fill in gaps in the evolutionary history of lineages like Microcachrys, which we demonstrate occurred in the Northern hemisphere before becoming restricted to its current range (Tasmania).

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