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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

Divergent vs. convergent evolution of the molecular fingerprints of mature chondrocytes and osteoblasts. Venn Diagrams comparing putative molecular fingerprints between mature chondrocytes and osteoblasts in three distinct vertebrate clades may resolve among two hypotheses for the origins of the osteoblast. (A) Divergent model. Osteoblast evolved when a GRN was co-opted from mature chondrocytes. Differing selective pressures on ancestors of various lineages, followed by lineage-specific constraints, may have caused gradual divergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between mature chondrocyte and osteoblast molecular fingerprints will be significantly higher in earlier diverged lineages, such as teleosts, than in later diverged lineages, such as mammals. (B) Convergent model. Osteoblast GRN evolved de novo. Similar selective pressures on osteoblasts and mature chondrocytes in ancestors of later diverging lineages may have caused convergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between molecular fingerprints of mature chondrocytes and osteoblasts will be significantly lower in earlier evolved lineages. Branch lengths in trees are arbitrary; the overlap between molecular fingerprints is shown in green and, in the divergent model, may represent the ancestral GRN kernel of both mature chondrocyte and osteoblast.
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Figure 5: Divergent vs. convergent evolution of the molecular fingerprints of mature chondrocytes and osteoblasts. Venn Diagrams comparing putative molecular fingerprints between mature chondrocytes and osteoblasts in three distinct vertebrate clades may resolve among two hypotheses for the origins of the osteoblast. (A) Divergent model. Osteoblast evolved when a GRN was co-opted from mature chondrocytes. Differing selective pressures on ancestors of various lineages, followed by lineage-specific constraints, may have caused gradual divergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between mature chondrocyte and osteoblast molecular fingerprints will be significantly higher in earlier diverged lineages, such as teleosts, than in later diverged lineages, such as mammals. (B) Convergent model. Osteoblast GRN evolved de novo. Similar selective pressures on osteoblasts and mature chondrocytes in ancestors of later diverging lineages may have caused convergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between molecular fingerprints of mature chondrocytes and osteoblasts will be significantly lower in earlier evolved lineages. Branch lengths in trees are arbitrary; the overlap between molecular fingerprints is shown in green and, in the divergent model, may represent the ancestral GRN kernel of both mature chondrocyte and osteoblast.

Mentions: Two related, fascinating questions remain for future research: how did the GRNs directing skeletal cell differentiation appear, and how did they evolve afterward? In this review, we argue that gradual establishment of the Runx2 GRN during evolution of the mature chondrocyte (subsequently co-opted by a non-chondrogenic mesenchymal cell to form bone) is more parsimonious than the de novo appearance of the Runx2 GRN in osteoblasts (Figure 4). Given the latter possibility, however, the tremendous gene expression similarities between mature cartilage and bone in tetrapods also may reflect co-option of the Runx2 GRN by the mature chondrocyte after it was established in the osteoblast. These possibilities predict divergent vs. convergent evolution, respectively, of the Runx2 GRN in mature chondrocytes after the appearance of the osteoblast. Therefore, we propose an examination of skeletal cell molecular fingerprints in a variety of vertebrates to resolve this issue. Our divergent model predicts that the overlap between mature chondrocyte and osteoblast molecular fingerprints will decrease in more recently evolved organisms (Figure 5A). For example, molecular fingerprints of mature chondrocytes and osteoblasts would overlap more in earlier diverged lineages of vertebrates, such as teleosts, than in later evolved lineages, such as amphibians or mammals. On the other hand, the convergent model predicts the opposite result (Figure 5B).


On the evolutionary relationship between chondrocytes and osteoblasts.

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

Divergent vs. convergent evolution of the molecular fingerprints of mature chondrocytes and osteoblasts. Venn Diagrams comparing putative molecular fingerprints between mature chondrocytes and osteoblasts in three distinct vertebrate clades may resolve among two hypotheses for the origins of the osteoblast. (A) Divergent model. Osteoblast evolved when a GRN was co-opted from mature chondrocytes. Differing selective pressures on ancestors of various lineages, followed by lineage-specific constraints, may have caused gradual divergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between mature chondrocyte and osteoblast molecular fingerprints will be significantly higher in earlier diverged lineages, such as teleosts, than in later diverged lineages, such as mammals. (B) Convergent model. Osteoblast GRN evolved de novo. Similar selective pressures on osteoblasts and mature chondrocytes in ancestors of later diverging lineages may have caused convergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between molecular fingerprints of mature chondrocytes and osteoblasts will be significantly lower in earlier evolved lineages. Branch lengths in trees are arbitrary; the overlap between molecular fingerprints is shown in green and, in the divergent model, may represent the ancestral GRN kernel of both mature chondrocyte and osteoblast.
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Figure 5: Divergent vs. convergent evolution of the molecular fingerprints of mature chondrocytes and osteoblasts. Venn Diagrams comparing putative molecular fingerprints between mature chondrocytes and osteoblasts in three distinct vertebrate clades may resolve among two hypotheses for the origins of the osteoblast. (A) Divergent model. Osteoblast evolved when a GRN was co-opted from mature chondrocytes. Differing selective pressures on ancestors of various lineages, followed by lineage-specific constraints, may have caused gradual divergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between mature chondrocyte and osteoblast molecular fingerprints will be significantly higher in earlier diverged lineages, such as teleosts, than in later diverged lineages, such as mammals. (B) Convergent model. Osteoblast GRN evolved de novo. Similar selective pressures on osteoblasts and mature chondrocytes in ancestors of later diverging lineages may have caused convergence between the GRN of osteoblasts and mature chondrocytes during vertebrate evolution. If true, then the overlap between molecular fingerprints of mature chondrocytes and osteoblasts will be significantly lower in earlier evolved lineages. Branch lengths in trees are arbitrary; the overlap between molecular fingerprints is shown in green and, in the divergent model, may represent the ancestral GRN kernel of both mature chondrocyte and osteoblast.
Mentions: Two related, fascinating questions remain for future research: how did the GRNs directing skeletal cell differentiation appear, and how did they evolve afterward? In this review, we argue that gradual establishment of the Runx2 GRN during evolution of the mature chondrocyte (subsequently co-opted by a non-chondrogenic mesenchymal cell to form bone) is more parsimonious than the de novo appearance of the Runx2 GRN in osteoblasts (Figure 4). Given the latter possibility, however, the tremendous gene expression similarities between mature cartilage and bone in tetrapods also may reflect co-option of the Runx2 GRN by the mature chondrocyte after it was established in the osteoblast. These possibilities predict divergent vs. convergent evolution, respectively, of the Runx2 GRN in mature chondrocytes after the appearance of the osteoblast. Therefore, we propose an examination of skeletal cell molecular fingerprints in a variety of vertebrates to resolve this issue. Our divergent model predicts that the overlap between mature chondrocyte and osteoblast molecular fingerprints will decrease in more recently evolved organisms (Figure 5A). For example, molecular fingerprints of mature chondrocytes and osteoblasts would overlap more in earlier diverged lineages of vertebrates, such as teleosts, than in later evolved lineages, such as amphibians or mammals. On the other hand, the convergent model predicts the opposite result (Figure 5B).

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