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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 the appearance of the GRN driving osteoblast formation. (A) In this scenario, the osteoblast (and the Runx2 GRN that drives its formation) appeared de novo, independent of the chondrocyte. This model is consistent with saltational evolution, in which large-scale genomic changes may facilitate the evolution of novelty over short periods of geologic time. (B) In an alternative scenario, the osteoblast appeared after a series of step-wise additions to the mature chondrocyte (and thus the Runx2 GRN that drives its formation). After establishment of the Runx2 GRN in mature chondrocytes, the osteoblast appeared when another population of cells co-opted the Runx2 GRN. This model is consistent with gradual evolution, in which a series of small changes over geologic time may facilitate the evolution of novelty. The size of the circles and polygons represent relative levels of up- or down-regulation of genes in the respective GRNs (see text for discussion of interactions between Sox9 and Runx2 GRNs).
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Figure 4: Differing models for the appearance of the GRN driving osteoblast formation. (A) In this scenario, the osteoblast (and the Runx2 GRN that drives its formation) appeared de novo, independent of the chondrocyte. This model is consistent with saltational evolution, in which large-scale genomic changes may facilitate the evolution of novelty over short periods of geologic time. (B) In an alternative scenario, the osteoblast appeared after a series of step-wise additions to the mature chondrocyte (and thus the Runx2 GRN that drives its formation). After establishment of the Runx2 GRN in mature chondrocytes, the osteoblast appeared when another population of cells co-opted the Runx2 GRN. This model is consistent with gradual evolution, in which a series of small changes over geologic time may facilitate the evolution of novelty. The size of the circles and polygons represent relative levels of up- or down-regulation of genes in the respective GRNs (see text for discussion of interactions between Sox9 and Runx2 GRNs).

Mentions: Combining evidence from traditional and modern studies, we hypothesize that the GRN underlying bone formation evolved from a GRN underlying mature cartilage formation (Figure 4). Functional, histological, embryological, and molecular similarities among immature cartilage, mature cartilage, and bone suggest that these tissues may share an evolutionary history (Figure 1). The fossil record, comparative anatomy, and embryology demonstrate that immature cartilage evolved first (Figure 2). When combined with molecular genetic data (Figure 3), this means that the first evolved skeletal GRN was dominated by the gene ancestral to Sox9, driving immature cartilage formation. This GRN likely involved genes ancestral to Runx2 in early phylogenetic (and ontogenetic) stages. In gnathostomes, a Runx2 GRN drives formation of both mature cartilage and bone (Figure 3), but how did this novel GRN evolve to produce these novel skeletal tissues?


On the evolutionary relationship between chondrocytes and osteoblasts.

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

Differing models for the appearance of the GRN driving osteoblast formation. (A) In this scenario, the osteoblast (and the Runx2 GRN that drives its formation) appeared de novo, independent of the chondrocyte. This model is consistent with saltational evolution, in which large-scale genomic changes may facilitate the evolution of novelty over short periods of geologic time. (B) In an alternative scenario, the osteoblast appeared after a series of step-wise additions to the mature chondrocyte (and thus the Runx2 GRN that drives its formation). After establishment of the Runx2 GRN in mature chondrocytes, the osteoblast appeared when another population of cells co-opted the Runx2 GRN. This model is consistent with gradual evolution, in which a series of small changes over geologic time may facilitate the evolution of novelty. The size of the circles and polygons represent relative levels of up- or down-regulation of genes in the respective GRNs (see text for discussion of interactions between Sox9 and Runx2 GRNs).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585068&req=5

Figure 4: Differing models for the appearance of the GRN driving osteoblast formation. (A) In this scenario, the osteoblast (and the Runx2 GRN that drives its formation) appeared de novo, independent of the chondrocyte. This model is consistent with saltational evolution, in which large-scale genomic changes may facilitate the evolution of novelty over short periods of geologic time. (B) In an alternative scenario, the osteoblast appeared after a series of step-wise additions to the mature chondrocyte (and thus the Runx2 GRN that drives its formation). After establishment of the Runx2 GRN in mature chondrocytes, the osteoblast appeared when another population of cells co-opted the Runx2 GRN. This model is consistent with gradual evolution, in which a series of small changes over geologic time may facilitate the evolution of novelty. The size of the circles and polygons represent relative levels of up- or down-regulation of genes in the respective GRNs (see text for discussion of interactions between Sox9 and Runx2 GRNs).
Mentions: Combining evidence from traditional and modern studies, we hypothesize that the GRN underlying bone formation evolved from a GRN underlying mature cartilage formation (Figure 4). Functional, histological, embryological, and molecular similarities among immature cartilage, mature cartilage, and bone suggest that these tissues may share an evolutionary history (Figure 1). The fossil record, comparative anatomy, and embryology demonstrate that immature cartilage evolved first (Figure 2). When combined with molecular genetic data (Figure 3), this means that the first evolved skeletal GRN was dominated by the gene ancestral to Sox9, driving immature cartilage formation. This GRN likely involved genes ancestral to Runx2 in early phylogenetic (and ontogenetic) stages. In gnathostomes, a Runx2 GRN drives formation of both mature cartilage and bone (Figure 3), but how did this novel GRN evolve to produce these novel skeletal tissues?

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