On the Dissociability of the Fundamental Processes in Ontogenesis

Needham, Joseph

doi:10.1111/j.1469-185x.1933.tb01153.x

Cited by 133 publications

(71 citation statements)

References 110 publications

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“…Spatially localized control of cell proliferation by Hh signaling along the ventral Op controls two parameters of morphogenesis: vp edge length and overall ventral outgrowth. The ability of a local signal to alter specifically a local region of morphology of a given bone is consistent with the concept of dissociability, which proposes that functional or developmental units, normally integrated, might be experimentally separated from one another (Needham, 1933). Genetically based modular organization (Raff and Raff, 2000), as we observe in the Op, allows regional rates of bone growth to be individually regulated so as not to have morphogenetic consequences in other regions of the bone.…”

Section: Modular Basis Of Op Morphogenesissupporting

confidence: 52%

Hedgehog-dependent proliferation drives modular growth during morphogenesis of a dermal bone

2012

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SUMMARYIn the developing skeleton, dermal bone morphogenesis includes the balanced proliferation, recruitment and differentiation of osteoblast precursors, yet how bones acquire unique morphologies is unknown. We show that Hedgehog (Hh) signaling mediates bone shaping during early morphogenesis of the opercle (Op), a well characterized dermal bone of the zebrafish craniofacial skeleton. ihha is specifically expressed in a local population of active osteoblasts along the principal growing edge of the bone. Mutational studies show that Hh signaling by this osteoblast population is both necessary and sufficient for full recruitment of pre-osteoblasts into the signaling population. Loss of ihha function results in locally reduced proliferation of pre-osteoblasts and consequent reductions in recruitment into the osteoblast pool, reduced bone edge length and reduced outgrowth. Conversely, hyperactive Hh signaling in ptch1 mutants causes opposite defects in proliferation and growth. Time-lapse microscopy of early Op morphogenesis using transgenically labeled osteoblasts demonstrates that ihha-dependent bone development is not only region specific, but also begins exactly at the onset of a second phase of morphogenesis, when the early bone begins to reshape into a more complex form. These features strongly support a hypothesis that dermal bone development is modular, with different gene sets functioning at specific times and locations to pattern growth. The Hh-dependent module is not limited to this second phase of bone growth: during later larval development, the Op is fused along the dysmorphic edge to adjacent dermal bones. Hence, patterning within a module may include adjacent regions of functionally related bones and might require that signaling pathways function over an extended period of development.

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Section: Modular Basis Of Op Morphogenesissupporting

confidence: 52%

Hedgehog-dependent proliferation drives modular growth during morphogenesis of a dermal bone

2012

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“…6, 14, 26, and 27). Because morphological development is extensively if not universally mediated by binary switches (14), modularity was recognized early as a feature of morphology (28). Phenotypic modularity is implied by the familiar word ''trait.''…”

mentioning

confidence: 99%

“…Modular dissociability, or the propensity for independent variation and shuffling of structural traits during evolution, has been noted in embryology (28), molecular biology (33), and paleontology (34). Vermeij (34) identified the evolutionary versatility of a lineage with the number of independently variable components of its phenotype.…”

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confidence: 99%

Evolution in the light of developmental and cell biology, and vice versa

West‐Eberhard

1998

Proc. Natl. Acad. Sci. U.S.A.

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“…This characteristic feature of all organisms is named modularity, and it is likely to be important for adaptive phenotypic evolution, allowing optimization of different traits individually by natural selection (1). The dissociability of such modules in evolution is believed to be facilitated by a corresponding modular organization of interacting proteins controlling their development, such that changes that occur within one module have less chance of impacting negatively on others (2).…”

mentioning

confidence: 99%

The role of the proline-rich domain of Ssdp1 in the modular architecture of the vertebrate head organizer

Enkhmandakh

Makeyev²,

Bayarsaihan³

2006

Proc. Natl. Acad. Sci. U.S.A.

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Lim1, Ssdp1, and Ldb1 proteins are components of the Ldb1-associated transcriptional complex, which is important in the head-organizing activity during early mouse development. Depletion of each individual protein alone causes a headless phenotype. To explore in more detail the modular architecture of the complex, we have generated two different gene-trapped mouse lines that express truncated forms of Ssdp1. Embryos derived from the gene-trapped line that encodes a truncated Ssdp1 lacking the proline-rich sequence exhibit a lethal abnormal head-development phenotype, resembling mouse embryos deficient for Lim1, Ssdp1, or Otx2 genes. Embryos derived from the second gene-trapped line, in which most of the proline-rich domain of Ssdp1 is retained, did not show abnormalities in head development. Our data demonstrate that components of the Ldb1-dependent module can be subdivided further into discrete functional domains and that the proline-rich stretch of Ssdp1 is critical for embryonic head development. Furthermore, phylogenetic comparisons revealed that in Caenorhabditis elegans, a similar proline-rich sequence is absent in Ssdp but present in Ldb1. We conclude that although the overall architecture of the Ldb1-dependent module has been preserved, the genetic specification of its individual components has diversified during evolution, without compromising the function of the module.gene trap ͉ Ldb1 ͉ module

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On the Dissociability of the Fundamental Processes in Ontogenesis

Cited by 133 publications

References 110 publications

Hedgehog-dependent proliferation drives modular growth during morphogenesis of a dermal bone

Hedgehog-dependent proliferation drives modular growth during morphogenesis of a dermal bone

Evolution in the light of developmental and cell biology, and vice versa

The role of the proline-rich domain of Ssdp1 in the modular architecture of the vertebrate head organizer

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