nkx3.2 mutant zebrafish accommodate jaw joint loss through a phenocopy of the head shapes of Paleozoic jawless fish
The vertebrate jaw is a versatile feeding apparatus. To function, it requires a joint between the upper and lower jaws, so jaw joint defects are often highly disruptive and difficult to study. To describe the consequences of jaw-joint dysfunction, we engineered two independent null alleles of a sing...
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Published in | Journal of experimental biology |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
01.01.2020
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Abstract | The vertebrate jaw is a versatile feeding apparatus. To function, it requires a joint between the upper and lower jaws, so jaw joint defects are often highly disruptive and difficult to study. To describe the consequences of jaw-joint dysfunction, we engineered two independent null alleles of a single jaw-joint marker gene, nkx3.2, in zebrafish. These mutations caused zebrafish to become functionally jawless via fusion of the upper and lower jaw cartilages (ankylosis). Despite lacking jaw joints, nkx3.2 mutants survived to adulthood and accommodate this defect by: a) having a remodelled skull with a fixed open gape, reduced snout, and enlarged branchial region; and b) performing ram feeding in the absence of jaw-generated suction. The late onset and broad extent of phenotypic changes in the mutants suggest that modifications to the skull are induced by functional agnathia, secondarily to nkx3.2 loss-of-function. Interestingly, nkx3.2 mutants superficially resemble ancient jawless vertebrates (anaspids and furcacaudiid thelodonts) in overall head shapes. Because no homology exists in individual skull elements between these taxa, the adult nkx3.2 phenotype is not a reversal, but convergence due to similar functional requirements of feeding without moveable jaws. This remarkable analogy strongly suggests that jaw movements themselves dramatically influence the development of jawed vertebrate skulls. Thus, these mutants provide a unique model with which to: a) investigate adaptive responses to perturbation in skeletal development; b) re-evaluate evolutionarily inspired interpretations of phenocopies generated by gene knockdowns and knockouts; and c) gain insights into feeding mechanics of the extinct agnathans. |
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AbstractList | The vertebrate jaw is a versatile feeding apparatus. To function, it requires a joint between the upper and lower jaws, so jaw joint defects are often highly disruptive and difficult to study. To describe the consequences of jaw-joint dysfunction, we engineered two independent null alleles of a single jaw-joint marker gene, nkx3.2, in zebrafish. These mutations caused zebrafish to become functionally jawless via fusion of the upper and lower jaw cartilages (ankylosis). Despite lacking jaw joints, nkx3.2 mutants survived to adulthood and accommodate this defect by: a) having a remodelled skull with a fixed open gape, reduced snout, and enlarged branchial region; and b) performing ram feeding in the absence of jaw-generated suction. The late onset and broad extent of phenotypic changes in the mutants suggest that modifications to the skull are induced by functional agnathia, secondarily to nkx3.2 loss-of-function. Interestingly, nkx3.2 mutants superficially resemble ancient jawless vertebrates (anaspids and furcacaudiid thelodonts) in overall head shapes. Because no homology exists in individual skull elements between these taxa, the adult nkx3.2 phenotype is not a reversal, but convergence due to similar functional requirements of feeding without moveable jaws. This remarkable analogy strongly suggests that jaw movements themselves dramatically influence the development of jawed vertebrate skulls. Thus, these mutants provide a unique model with which to: a) investigate adaptive responses to perturbation in skeletal development; b) re-evaluate evolutionarily inspired interpretations of phenocopies generated by gene knockdowns and knockouts; and c) gain insights into feeding mechanics of the extinct agnathans. |
Author | Graf, Daniel Crump, J Gage Smeeton, Joanna Allison, W Ted Miyashita, Tetsuto Gordon, Brogan Baddam, Pranidhi Palmer, A Richard Oel, A Phil Natarajan, Natasha |
Author_xml | – sequence: 1 givenname: Tetsuto orcidid: 0000-0003-0050-4594 surname: Miyashita fullname: Miyashita, Tetsuto organization: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9 – sequence: 2 givenname: Pranidhi surname: Baddam fullname: Baddam, Pranidhi organization: Department of Dentistry, University of Alberta, Edmonton, Alberta, Canada T6G 2R3 – sequence: 3 givenname: Joanna surname: Smeeton fullname: Smeeton, Joanna organization: Department of Stem Cell Biology and Regenerative Medicine, W.M. Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA – sequence: 4 givenname: A Phil surname: Oel fullname: Oel, A Phil organization: Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, 69117, Germany – sequence: 5 givenname: Natasha surname: Natarajan fullname: Natarajan, Natasha organization: Department of Stem Cell Biology and Regenerative Medicine, W.M. Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA – sequence: 6 givenname: Brogan surname: Gordon fullname: Gordon, Brogan organization: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9 – sequence: 7 givenname: A Richard orcidid: 0000-0002-7579-3899 surname: Palmer fullname: Palmer, A Richard organization: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9 – sequence: 8 givenname: J Gage surname: Crump fullname: Crump, J Gage organization: Department of Stem Cell Biology and Regenerative Medicine, W.M. Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA – sequence: 9 givenname: Daniel surname: Graf fullname: Graf, Daniel organization: Department of Medical Genetics, University of Alberta, Edmonton, Alberta, Canada T6G 2R7 – sequence: 10 givenname: W Ted orcidid: 0000-0002-8461-4864 surname: Allison fullname: Allison, W Ted organization: Department of Medical Genetics, University of Alberta, Edmonton, Alberta, Canada T6G 2R7 |
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Keywords | Agnatha Jaw Skeletal remodeling Developmental plasticity Bapx Nkx3.2 Zebrafish Joint |
Language | English |
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Title | nkx3.2 mutant zebrafish accommodate jaw joint loss through a phenocopy of the head shapes of Paleozoic jawless fish |
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