Fgf-driven Tbx protein activities directly induce myf5 and myod to initiate zebrafish myogenesis

TY - JOUR

T1 - Fgf-driven Tbx protein activities directly induce myf5 and myod to initiate zebrafish myogenesis

AU - Osborn, Daniel P S

AU - Li, Kuoyu

AU - Cutty, Stephen J

AU - Nelson, Andrew C

AU - Wardle, Fiona C

AU - Hinits, Yaniv

AU - Hughes, Simon M

N1 - © 2020. Published by The Company of Biologists Ltd.

PY - 2020/4/28

Y1 - 2020/4/28

N2 - Skeletal muscle derives from dorsal mesoderm formed during vertebrate gastrulation. Fibroblast growth factor (Fgf) signalling cooperates with Tbx transcription factors to promote dorsal mesoderm formation, but their role in myogenesis has been unclear. Using zebrafish, we show that dorsally derived Fgf signals act through Tbx16 and Tbxta to induce slow and fast trunk muscle precursors at distinct dorsoventral positions. Tbx16 binds to and directly activates the myf5 and myod genes, which are required for commitment to myogenesis. Tbx16 activity depends on Fgf signalling from the organiser. In contrast, Tbxta is not required for myf5 expression, but binds a specific site upstream of myod that is not bound by Tbx16 and drives (dependent on Fgf signals) myod expression in adaxial slow precursors, thereby initiating trunk myogenesis. After gastrulation, when similar muscle cell populations in the post-anal tail are generated from tailbud, declining Fgf signalling is less effective at initiating adaxial myogenesis, which is instead initiated by Hedgehog signalling from the notochord. Our findings suggest a hypothesis for ancestral vertebrate trunk myogenic patterning and how it was co-opted during tail evolution to generate similar muscle by new mechanisms.

AB - Skeletal muscle derives from dorsal mesoderm formed during vertebrate gastrulation. Fibroblast growth factor (Fgf) signalling cooperates with Tbx transcription factors to promote dorsal mesoderm formation, but their role in myogenesis has been unclear. Using zebrafish, we show that dorsally derived Fgf signals act through Tbx16 and Tbxta to induce slow and fast trunk muscle precursors at distinct dorsoventral positions. Tbx16 binds to and directly activates the myf5 and myod genes, which are required for commitment to myogenesis. Tbx16 activity depends on Fgf signalling from the organiser. In contrast, Tbxta is not required for myf5 expression, but binds a specific site upstream of myod that is not bound by Tbx16 and drives (dependent on Fgf signals) myod expression in adaxial slow precursors, thereby initiating trunk myogenesis. After gastrulation, when similar muscle cell populations in the post-anal tail are generated from tailbud, declining Fgf signalling is less effective at initiating adaxial myogenesis, which is instead initiated by Hedgehog signalling from the notochord. Our findings suggest a hypothesis for ancestral vertebrate trunk myogenic patterning and how it was co-opted during tail evolution to generate similar muscle by new mechanisms.

KW - Fgf

KW - Hedgehog

KW - Muscle

KW - Myf5

KW - Myod

KW - Myogenin

KW - Myosin

KW - Ntl

KW - Spt

KW - Tbx16

KW - Tbxta

KW - Zebrafish

UR - http://www.scopus.com/inward/record.url?scp=85084170576&partnerID=8YFLogxK

U2 - 10.1242/dev.184689

DO - 10.1242/dev.184689

M3 - Article

C2 - 32345657

SN - 0950-1991

VL - 147

JO - Development

JF - Development

IS - 8

M1 - dev184689

ER -