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On the evolutionary relationship between chondrocytes and osteoblasts.

Gómez-Picos P, Eames BF - Front Genet (2015)

Bottom Line: Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage.We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively.Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, University of Saskatchewan, Saskatoon, SK Canada.

ABSTRACT
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. Here, we synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Since transcription factors are often core components of GRNs (i.e., kernels), we focus our analyses on Sox9 and Runx2. Our argument centers on three skeletal tissues that comprise the majority of the vertebrate skeleton: immature cartilage, mature cartilage, and bone. Immature cartilage is produced during early stages of cartilage differentiation and can persist into adulthood, whereas mature cartilage undergoes additional stages of differentiation, including hypertrophy and mineralization. Functionally, histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Intriguingly, the Sox9 GRN driving cartilage formation appears to be dominant to the Runx2 GRN of bone. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage. We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively. Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

No MeSH data available.


Related in: MedlinePlus

Differing models for levels of constraint and adaptation among skeletal cells of different vertebrate lineages. Venn diagrams comparing putative molecular fingerprints of chondrocytes and osteoblasts from three vertebrate clades. The ancestral chondrocyte and osteoblast GRN kernels are represented in the overlap of the circles. More overlap represents more constraint/less adaptation among clades. (A) The first scenario predicts that the molecular fingerprints of the chondrocyte and osteoblast (and thus the GRNs governing their formation) are constrained to equal extents among vertebrates (Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). (B) The second scenario predicts that the chondrocyte molecular fingerprint is more constrained among vertebrate clades, while the osteoblast molecular fingerprint shows more signs of clade-specific adaptations (Eames et al., 2012). In general, this latter scenario posits that a cell type appearing later during animal phylogeny is more free to vary than a cell type appearing earlier, whose molecular fingerprint was fixed via stabilizing selection.
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Figure 6: Differing models for levels of constraint and adaptation among skeletal cells of different vertebrate lineages. Venn diagrams comparing putative molecular fingerprints of chondrocytes and osteoblasts from three vertebrate clades. The ancestral chondrocyte and osteoblast GRN kernels are represented in the overlap of the circles. More overlap represents more constraint/less adaptation among clades. (A) The first scenario predicts that the molecular fingerprints of the chondrocyte and osteoblast (and thus the GRNs governing their formation) are constrained to equal extents among vertebrates (Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). (B) The second scenario predicts that the chondrocyte molecular fingerprint is more constrained among vertebrate clades, while the osteoblast molecular fingerprint shows more signs of clade-specific adaptations (Eames et al., 2012). In general, this latter scenario posits that a cell type appearing later during animal phylogeny is more free to vary than a cell type appearing earlier, whose molecular fingerprint was fixed via stabilizing selection.

Mentions: But do skeletal cell molecular fingerprints evolve in clade-specific manners? A limited number of studies trying to answer this question suggest two competing ideas. On the one hand, molecular fingerprints of the chondrocyte and the osteoblast have been proposed to be highly constrained among various vertebrate clades (Figure 6A; Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). On the other hand, gene expression comparisons between gar, zebrafish, chick, and mouse suggest that the chondrocyte molecular fingerprint is constrained among vertebrates, while the osteoblast molecular fingerprint varied, perhaps in response to clade-specific selective pressures (Figure 6B; Eames et al., 2012). Interestingly, generalizing these results puts forward the hypothesis that earlier-evolved cell types, in this case chondrocytes, might be more constrained in their gene expression than cell types that appeared later, such as osteoblasts, perhaps due to stabilizing selection over geologic timescales. Comparative transcriptomics can quantitate constraint and adaptation, by measuring how transcript levels vary among samples from different taxonomic lineages.


On the evolutionary relationship between chondrocytes and osteoblasts.

Gómez-Picos P, Eames BF - Front Genet (2015)

Differing models for levels of constraint and adaptation among skeletal cells of different vertebrate lineages. Venn diagrams comparing putative molecular fingerprints of chondrocytes and osteoblasts from three vertebrate clades. The ancestral chondrocyte and osteoblast GRN kernels are represented in the overlap of the circles. More overlap represents more constraint/less adaptation among clades. (A) The first scenario predicts that the molecular fingerprints of the chondrocyte and osteoblast (and thus the GRNs governing their formation) are constrained to equal extents among vertebrates (Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). (B) The second scenario predicts that the chondrocyte molecular fingerprint is more constrained among vertebrate clades, while the osteoblast molecular fingerprint shows more signs of clade-specific adaptations (Eames et al., 2012). In general, this latter scenario posits that a cell type appearing later during animal phylogeny is more free to vary than a cell type appearing earlier, whose molecular fingerprint was fixed via stabilizing selection.
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Related In: Results  -  Collection

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Figure 6: Differing models for levels of constraint and adaptation among skeletal cells of different vertebrate lineages. Venn diagrams comparing putative molecular fingerprints of chondrocytes and osteoblasts from three vertebrate clades. The ancestral chondrocyte and osteoblast GRN kernels are represented in the overlap of the circles. More overlap represents more constraint/less adaptation among clades. (A) The first scenario predicts that the molecular fingerprints of the chondrocyte and osteoblast (and thus the GRNs governing their formation) are constrained to equal extents among vertebrates (Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). (B) The second scenario predicts that the chondrocyte molecular fingerprint is more constrained among vertebrate clades, while the osteoblast molecular fingerprint shows more signs of clade-specific adaptations (Eames et al., 2012). In general, this latter scenario posits that a cell type appearing later during animal phylogeny is more free to vary than a cell type appearing earlier, whose molecular fingerprint was fixed via stabilizing selection.
Mentions: But do skeletal cell molecular fingerprints evolve in clade-specific manners? A limited number of studies trying to answer this question suggest two competing ideas. On the one hand, molecular fingerprints of the chondrocyte and the osteoblast have been proposed to be highly constrained among various vertebrate clades (Figure 6A; Fisher and Franz-Odendaal, 2012; Vieira et al., 2013). On the other hand, gene expression comparisons between gar, zebrafish, chick, and mouse suggest that the chondrocyte molecular fingerprint is constrained among vertebrates, while the osteoblast molecular fingerprint varied, perhaps in response to clade-specific selective pressures (Figure 6B; Eames et al., 2012). Interestingly, generalizing these results puts forward the hypothesis that earlier-evolved cell types, in this case chondrocytes, might be more constrained in their gene expression than cell types that appeared later, such as osteoblasts, perhaps due to stabilizing selection over geologic timescales. Comparative transcriptomics can quantitate constraint and adaptation, by measuring how transcript levels vary among samples from different taxonomic lineages.

Bottom Line: Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage.We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively.Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, University of Saskatchewan, Saskatoon, SK Canada.

ABSTRACT
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. Here, we synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Since transcription factors are often core components of GRNs (i.e., kernels), we focus our analyses on Sox9 and Runx2. Our argument centers on three skeletal tissues that comprise the majority of the vertebrate skeleton: immature cartilage, mature cartilage, and bone. Immature cartilage is produced during early stages of cartilage differentiation and can persist into adulthood, whereas mature cartilage undergoes additional stages of differentiation, including hypertrophy and mineralization. Functionally, histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Intriguingly, the Sox9 GRN driving cartilage formation appears to be dominant to the Runx2 GRN of bone. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage. We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively. Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.

No MeSH data available.


Related in: MedlinePlus