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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

Clues to the evolutionary relationship between the chondrocyte and osteoblast emerge from analyses of the fossil record and comparative anatomy. (A) Appearance of immature cartilage, mature cartilage, and bone from available fossil record. These data indicate clearly that immature cartilage appeared first, then mature cartilage and bone. By extension, the chondrocyte preceded the osteoblast during evolution. (B) Extant taxa with at least one species containing cartilage or cartilage-like tissues, which are non-mineralized outside of vertebrates. These data suggest that a GRN driving differentiation of an immature chondrocyte evolved first, and then became established in the genome of chordates (along with the notochord, a cartilage-like tissue). Subsequently, this GRN was modified by another GRN that drove differentiation of a mature chondrocyte (and osteoblast) within vertebrates. Branch lengths in trees are arbitrary; dashed lines indicate extinct taxa.
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Figure 2: Clues to the evolutionary relationship between the chondrocyte and osteoblast emerge from analyses of the fossil record and comparative anatomy. (A) Appearance of immature cartilage, mature cartilage, and bone from available fossil record. These data indicate clearly that immature cartilage appeared first, then mature cartilage and bone. By extension, the chondrocyte preceded the osteoblast during evolution. (B) Extant taxa with at least one species containing cartilage or cartilage-like tissues, which are non-mineralized outside of vertebrates. These data suggest that a GRN driving differentiation of an immature chondrocyte evolved first, and then became established in the genome of chordates (along with the notochord, a cartilage-like tissue). Subsequently, this GRN was modified by another GRN that drove differentiation of a mature chondrocyte (and osteoblast) within vertebrates. Branch lengths in trees are arbitrary; dashed lines indicate extinct taxa.

Mentions: Traditional studies, such as the fossil record, comparative anatomy, and embryology, demonstrate that the first skeletal tissue to evolve was immature cartilage (Figure 2). The fossil record reveals a great diversity of mineralized tissues about 500 million years ago (Mya; Janvier, 1996, 2015; Donoghue and Sansom, 2002; Donoghue et al., 2006), suggesting that GRNs of skeletal histogenesis were undergoing an adaptive radiation. So which skeletal tissue appeared first in the fossil record? This question is complicated by the facts that currently discovered fossils may represent a biased fraction of ancestral tissues, and that non-mineralized, lightly mineralized, or transiently mineralized tissues likely are not preserved well in the fossil record. Despite these limitations, however, the oldest skeletal tissue in the fossil record is unmineralized cartilage in the chordate fossil Haikouella from 530 Mya (Figure 2A; Mallatt and Chen, 2003). Many specimens preserving soft tissues of this incredibly important fossil have been found, but they appear to be represented only in a small region of the Yunnan province in China (Chen et al., 1999), reflecting potential bias in the fossil record.


On the evolutionary relationship between chondrocytes and osteoblasts.

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

Clues to the evolutionary relationship between the chondrocyte and osteoblast emerge from analyses of the fossil record and comparative anatomy. (A) Appearance of immature cartilage, mature cartilage, and bone from available fossil record. These data indicate clearly that immature cartilage appeared first, then mature cartilage and bone. By extension, the chondrocyte preceded the osteoblast during evolution. (B) Extant taxa with at least one species containing cartilage or cartilage-like tissues, which are non-mineralized outside of vertebrates. These data suggest that a GRN driving differentiation of an immature chondrocyte evolved first, and then became established in the genome of chordates (along with the notochord, a cartilage-like tissue). Subsequently, this GRN was modified by another GRN that drove differentiation of a mature chondrocyte (and osteoblast) within vertebrates. Branch lengths in trees are arbitrary; dashed lines indicate extinct taxa.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Clues to the evolutionary relationship between the chondrocyte and osteoblast emerge from analyses of the fossil record and comparative anatomy. (A) Appearance of immature cartilage, mature cartilage, and bone from available fossil record. These data indicate clearly that immature cartilage appeared first, then mature cartilage and bone. By extension, the chondrocyte preceded the osteoblast during evolution. (B) Extant taxa with at least one species containing cartilage or cartilage-like tissues, which are non-mineralized outside of vertebrates. These data suggest that a GRN driving differentiation of an immature chondrocyte evolved first, and then became established in the genome of chordates (along with the notochord, a cartilage-like tissue). Subsequently, this GRN was modified by another GRN that drove differentiation of a mature chondrocyte (and osteoblast) within vertebrates. Branch lengths in trees are arbitrary; dashed lines indicate extinct taxa.
Mentions: Traditional studies, such as the fossil record, comparative anatomy, and embryology, demonstrate that the first skeletal tissue to evolve was immature cartilage (Figure 2). The fossil record reveals a great diversity of mineralized tissues about 500 million years ago (Mya; Janvier, 1996, 2015; Donoghue and Sansom, 2002; Donoghue et al., 2006), suggesting that GRNs of skeletal histogenesis were undergoing an adaptive radiation. So which skeletal tissue appeared first in the fossil record? This question is complicated by the facts that currently discovered fossils may represent a biased fraction of ancestral tissues, and that non-mineralized, lightly mineralized, or transiently mineralized tissues likely are not preserved well in the fossil record. Despite these limitations, however, the oldest skeletal tissue in the fossil record is unmineralized cartilage in the chordate fossil Haikouella from 530 Mya (Figure 2A; Mallatt and Chen, 2003). Many specimens preserving soft tissues of this incredibly important fossil have been found, but they appear to be represented only in a small region of the Yunnan province in China (Chen et al., 1999), reflecting potential bias in the fossil record.

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