Coordinated patterning of zebrafish caudal fin symmetry by a central and two peripheral organizers.
actinopterygian
caudal fin
fin rays
fin symmetry
hypural diastema
teleosts
Journal
Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
revised:
17
03
2022
received:
29
12
2021
accepted:
03
04
2022
pubmed:
12
4
2022
medline:
3
8
2022
entrez:
11
4
2022
Statut:
ppublish
Résumé
Caudal fin symmetry characterizes teleosts and likely contributes to their evolutionary success. However, the coordinated development and patterning of skeletal elements establishing external symmetry remains incompletely understood. We explore the spatiotemporal emergence of caudal skeletal elements in zebrafish to consider evolutionary and developmental origins of caudal fin symmetry. Transgenic reporters and skeletal staining reveal that the hypural diastema-defining gap between hypurals 2 and 3 forms early and separates progenitors of two plates of connective tissue. Two sets of central principal rays (CPRs) synchronously, sequentially, and symmetrically emerge around the diastema. The two dorsal- and ventral-most rays (peripheral principal rays, PPRs) arise independently and earlier than adjacent CPRs. Muscle and tendon markers reveal that different muscles attach to CPR and PPR sets. We propose that caudal fin symmetry originates from a central organizer that establishes the hypural diastema and bidirectionally patterns surrounding tissue into two plates of connective tissue and two mirrored sets of CPRs. Further, two peripheral organizers unidirectionally specify PPRs, forming a symmetric "composite" fin derived from three fields. Distinct CPR and PPR ontogenies may represent developmental modules conferring ray identities, muscle connections, and biomechanical properties. Our model contextualizes mechanistic studies of teleost fin morphological variation.
Sections du résumé
BACKGROUND
Caudal fin symmetry characterizes teleosts and likely contributes to their evolutionary success. However, the coordinated development and patterning of skeletal elements establishing external symmetry remains incompletely understood. We explore the spatiotemporal emergence of caudal skeletal elements in zebrafish to consider evolutionary and developmental origins of caudal fin symmetry.
RESULTS
Transgenic reporters and skeletal staining reveal that the hypural diastema-defining gap between hypurals 2 and 3 forms early and separates progenitors of two plates of connective tissue. Two sets of central principal rays (CPRs) synchronously, sequentially, and symmetrically emerge around the diastema. The two dorsal- and ventral-most rays (peripheral principal rays, PPRs) arise independently and earlier than adjacent CPRs. Muscle and tendon markers reveal that different muscles attach to CPR and PPR sets.
CONCLUSIONS
We propose that caudal fin symmetry originates from a central organizer that establishes the hypural diastema and bidirectionally patterns surrounding tissue into two plates of connective tissue and two mirrored sets of CPRs. Further, two peripheral organizers unidirectionally specify PPRs, forming a symmetric "composite" fin derived from three fields. Distinct CPR and PPR ontogenies may represent developmental modules conferring ray identities, muscle connections, and biomechanical properties. Our model contextualizes mechanistic studies of teleost fin morphological variation.
Identifiants
pubmed: 35403297
doi: 10.1002/dvdy.475
pmc: PMC9357109
mid: NIHMS1797176
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1306-1321Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM127761
Pays : United States
Organisme : NIGMS NIH HHS
ID : F31 GM139343
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007413
Pays : United States
Organisme : NIH HHS
ID : R01 OD011116
Pays : United States
Organisme : NIDCR NIH HHS
ID : R01 DE029193
Pays : United States
Organisme : NIDCR NIH HHS
ID : K99 DE024190
Pays : United States
Organisme : NIDCR NIH HHS
ID : R00 DE024190
Pays : United States
Informations de copyright
© 2022 American Association for Anatomy.
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