Reiterative use of FGF signaling in mesoderm development during embryogenesis and metamorphosis in the hemichordate Ptychodera flava

Abstract

BackgroundMesoderm is generally considered to be a germ layer that is unique to Bilateria, and it develops into diverse tissues, including muscle, and in the case of vertebrates, the skeleton and notochord. Studies on various deuterostome animals have demonstrated that fibroblast growth factor (FGF) signaling is required for the formation of many mesodermal structures, such as vertebrate somites, from which muscles are differentiated, and muscles in sea urchin embryos, suggesting an ancient role of FGF signaling in muscle development. However, the formation of trunk muscles in invertebrate chordates is FGF-independent, leading to ambiguity about this ancient role in deuterostomes. To further understand the role of FGF signaling during deuterostome evolution, we investigated the development of mesodermal structures during embryogenesis and metamorphosis in Ptychodera flava, an indirect-developing hemichordate that has larval morphology similar to echinoderms and adult body features that are similar to chordates.ResultsHere we show that genes encoding FGF ligands, FGF receptors and transcription factors that are known to be involved in mesoderm formation and myogenesis are expressed dynamically during embryogenesis and metamorphosis. FGF signaling at the early gastrula stage is required for the specification of the mesodermal cell fate in P. flava. The mesoderm cells are then differentiated stepwise into the hydroporic canal, the pharyngeal muscle and the muscle string; formation of the last two muscular structures are controlled by FGF signaling. Moreover, augmentation of FGF signaling during metamorphosis accelerated the process, facilitating the transformation from cilia-driven swimming larvae into muscle-driven worm-like juveniles.ConclusionsOur data show that FGF signaling is required for mesoderm induction and myogenesis in the P. flava embryo, and it is reiteratively used for the morphological transition during metamorphosis. The dependence of muscle development on FGF signaling in both planktonic larvae and sand-burrowing worms supports its ancestral role in deuterostomes.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1235-9) contains supplementary material, which is available to authorized users.

FGF signaling acts on different levels of mesoderm development within Spiralia

“…FGF signaling is required for the formation of all or most mesoderm, e.g. in hemichordates ( Fan et al, 2018 ; Green et al, 2013 ) and tunicates ( Davidson et al, 2006 ; Imai et al, 2002 ; Kim and Nishida, 2001 ; Yasuo and Hudson, 2007 ), or a subset of mesoderm, e.g. in vertebrates ( Amaya et al, 1993 ; Draper et al, 2003 ; Fletcher et al, 2006 ; Fletcher and Harland, 2008 ; Yamaguchi et al, 1994 ), cephalochordates ( Bertrand et al, 2011 ), sea urchins ( Andrikou et al, 2015 ) and nematodes ( Photos et al, 2006 ) (Fig.…”

“…In addition to shared sets of transcriptions factors, conserved signaling cascades are also involved in different steps of mesoderm development, such as fibroblast growth factor (FGF), Notch and bone morphogenetic protein (BMP) ( Good et al, 2004 ; Itoh and Ornitz, 2004 ; Sweet et al, 1999 ; Wijesena et al, 2017 ; Winnier et al, 1995 ) ( ). FGF signaling is of particular interest due to its proposed ancestral role in mesoderm induction in deuterostomes ( Fan et al, 2018 ; Green et al, 2013 ). Functional studies have demonstrated that this signal is required for posterior mesoderm formation in vertebrates ( Amaya et al, 1993 ; Draper et al, 2003 ; Fletcher et al, 2006 ; Fletcher and Harland, 2008 ; Yamaguchi et al, 1994 ), anterior mesoderm formation in cephalochordates ( Bertrand et al, 2011 ), mesenchyme induction and formation of notochord, trunk ventral cells (TVC) and tail muscle in tunicates ( Davidson et al, 2006 ; Imai et al, 2002 ; Kim and Nishida, 2001 ; Yasuo and Hudson, 2007 ), mesoderm induction in hemichordates ( Fan et al, 2018 ; Green et al, 2013 ) and myoblast formation in sea urchins ( Andrikou et al, 2015 ).…”

FGF signaling induces mesoderm in members of Spiralia

“…FGF signaling is required for the formation of all or most mesoderm e.g. in hemichordates (Fan et al, 2018;Green et al, 2013) and tunicates (Davidson et al, 2006;Imai et al, 2002;Kim and Nishida, 2001;Yasuo and Hudson, 2007), or a subset of mesoderm e.g. in vertebrates (Amaya et al, 1993;Draper et al, 2003;Fletcher et al, 2006;Fletcher and Harland, 2008;Yamaguchi et al, 1994), cephalochordates (Bertrand et al, 2011, sea urchins and nematodes (Photos et al, 2006) (S11).…”

“…Apart of shared sets of transcriptions factors, conserved signaling cascades are also involved in different steps of mesoderm development such as FGF, Notch and BMP (Good et al, 2004;Itoh and Ornitz, 2004;Sweet et al, 1999;Wijesena et al, 2017;Winnier et al, 1995). Among the aforementioned, FGF signaling is of particular interest due to its proposed ancestral role in mesoderm induction in deuterostomes (Fan et al, 2018;Green et al, 2013).…”

“…Functional studies have demonstrated that this signal is required for posterior mesoderm formation in vertebrates (Amaya et al, 1993;Draper et al, 2003;Fletcher et al, 2006;Fletcher and Harland, 2008;Yamaguchi et al, 1994), anterior mesoderm formation in cephalochordates (Bertrand et al, 2011), mesenchyme induction and formation of notochord, TVC and tail muscle in tunicates (Davidson et al, 2006;Imai et al, 2002;Kim and Nishida, 2001;Yasuo and Hudson, 2007), mesoderm induction in hemichordates (Fan et al, 2018;Green et al, 2013) and myoblast formation in sea urchins . Outside deuterostomes, however, studies addressing the role of FGF in mesoderm development are scarce.…”