scholarly journals biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila

2001 ◽  
Vol 15 (21) ◽  
pp. 2900-2915
Author(s):  
Stephane Zaffran ◽  
Axel Küchler ◽  
Hsiu-Hsiang Lee ◽  
Manfred Frasch

The subdivision of the lateral mesoderm into a visceral (splanchnic) and a somatic layer is a crucial event during early mesoderm development in both arthropod and vertebrate embryos. InDrosophila, this subdivision leads to the differential development of gut musculature versus body wall musculature. Here we report that biniou, the sole Drosophila representative of the FoxF subfamily of forkhead domain genes, has a key role in the development of the visceral mesoderm and the derived gut musculature.biniou expression is activated in the trunk visceral mesoderm primordia downstream of dpp, tinman, andbagpipe and is maintained in all types of developing gut muscles. We show that biniou activity is essential for maintaining the distinction between splanchnic and somatic mesoderm and for differentiation of the splanchnic mesoderm into midgut musculature.biniou is required not only for the activation of differentiation genes that are expressed ubiquitously in the trunk visceral mesoderm but also for the expression of dpp in parasegment 7, which governs proper midgut morphogenesis. Activation ofdpp is mediated by specific Biniou binding sites in adpp enhancer element, which suggests that Biniou serves as a tissue-specific cofactor of homeotic gene products in visceral mesoderm patterning. Based upon these and other data, we propose that the splanchnic mesoderm layers in Drosophila and vertebrate embryos are homologous structures whose development into gut musculature and other visceral organs is critically dependent on FoxF genes.

Development ◽  
1997 ◽  
Vol 124 (24) ◽  
pp. 4971-4982 ◽  
Author(s):  
Z. Yin ◽  
X.L. Xu ◽  
M. Frasch

The Drosophila tinman homeobox gene has a major role in early mesoderm patterning and determines the formation of visceral mesoderm, heart progenitors, specific somatic muscle precursors and glia-like mesodermal cells. These functions of tinman are reflected in its dynamic pattern of expression, which is characterized by initial widespread expression in the trunk mesoderm, then refinement to a broad dorsal mesodermal domain, and finally restricted expression in heart progenitors. Here we show that each of these phases of expression is driven by a discrete enhancer element, the first being active in the early mesoderm, the second in the dorsal mesoderm and the third in cardioblasts. We provide evidence that the early-active enhancer element is a direct target of twist, a gene encoding a basic helix-loop-helix (bHLH) protein, which is necessary for tinman activation. This 180 bp enhancer includes three E-box sequences which bind Twist protein in vitro and are essential for enhancer activity in vivo. Ectodermal misexpression of twist causes ectopic activation of this enhancer in ectodermal cells, indicating that twist is the only mesoderm-specific activator of early tinman expression. We further show that the 180 bp enhancer also includes negatively acting sequences. Binding of Even-skipped to these sequences appears to reduce twist-dependent activation in a periodic fashion, thus producing a striped tinman pattern in the early mesoderm. In addition, these sequences prevent activation of tinman by twist in a defined portion of the head mesoderm that gives rise to hemocytes. We find that this repression requires the function of buttonhead, a head-patterning gene, and that buttonhead is necessary for normal activation of the hematopoietic differentiation gene serpent in the same area. Together, our results show that tinman is controlled by an array of discrete enhancer elements that are activated successively by differential genetic inputs, as well as by closely linked activator and repressor binding sites within an early-acting enhancer, which restrict twist activity to specific areas within the twist expression domain.


Development ◽  
1998 ◽  
Vol 125 (4) ◽  
pp. 655-666 ◽  
Author(s):  
H.T. Broihier ◽  
L.A. Moore ◽  
M. Van Doren ◽  
S. Newman ◽  
R. Lehmann

In Drosophila as well as many vertebrate systems, germ cells form extraembryonically and migrate into the embryo before navigating toward gonadal mesodermal cells. How the gonadal mesoderm attracts migratory germ cells is not understood in any system. We have taken a genetic approach to identify genes required for germ cell migration in Drosophila. Here we describe the role of zfh-1 in germ cell migration to the gonadal mesoderm. In zfh-1 mutant embryos, the initial association of germ cells and gonadal mesoderm is blocked. Loss of zfh-1 activity disrupts the development of two distinct mesodermal populations: the caudal visceral mesoderm and the gonadal mesoderm. We demonstrate that the caudal visceral mesoderm facilitates the migration of germ cells from the endoderm to the mesoderm. Zfh-1 is also expressed in the gonadal mesoderm throughout the development of this tissue. Ectopic expression of Zfh-1 is sufficient to induce additional gonadal mesodermal cells and to alter the temporal course of gene expression within these cells. Finally, through analysis of a tinman zfh-1 double mutant, we show that zfh-1 acts in conjunction with tinman, another homeodomain protein, in the specification of lateral mesodermal derivatives, including the gonadal mesoderm.


Development ◽  
2000 ◽  
Vol 127 (17) ◽  
pp. 3695-3702 ◽  
Author(s):  
X. Yang ◽  
M. van Beest ◽  
H. Clevers ◽  
T. Jones ◽  
D.A. Hursh ◽  
...  

Drosophila T cell factor (dTcf) mediates transcriptional activation in the presence of Wingless signalling and repression in its absence. Wingless signalling is required for the correct expression of decapentaplegic (dpp), a Transforming Growth Factor (beta) family member, in parasegments 3 and 7 of the Drosophila visceral mesoderm. Here we demonstrate that a dpp enhancer element, which directs expression of a reporter gene in the visceral mesoderm in a pattern indistinguishable from dpp, has two functional dTcf binding sites. Mutations that reduce or eliminate Wingless signalling abolish dpp reporter gene expression in parasegment 3 and reduce it in parasegment 7 while ectopic expression of Wingless signalling components expand reporter gene expression anteriorly in the visceral mesoderm. However, mutation of the dTcf binding sites in the dpp enhancer results in ectopic expression of reporter gene expression throughout the visceral mesoderm, with no diminution of expression in the endogenous sites of expression. These results demonstrate that the primary function of dTcf binding to the dpp enhancer is repression throughout the visceral mesoderm and that activation by Wingless signalling is probably not mediated via these dTcf binding sites to facilitate correct dpp expression in the visceral mesoderm.


2020 ◽  
Author(s):  
Carmen Andrikou ◽  
Andreas Hejnol

AbstractFGF signaling is involved in mesoderm induction in deuterostomes, but not in flies and nematodes, where it has a role in mesoderm patterning and migration. However, comparable studies in other protostomic taxa are missing in order to decipher whether this mesoderm-inducing function of FGF extends beyond the lineage of deuterostomes. Here, we investigated the role of FGF signaling during mesoderm development in three species of lophophorates, a clade within the protostome group Spiralia. Our gene expression analyses show that the molecular patterning of mesoderm development is overall conserved between brachiopods and phoronids, but the spatial and temporal recruitment of transcription factors differs significantly. Moreover, inhibitor experiments demonstrate that FGF signaling is involved in mesoderm formation, morphogenetic movements of gastrulation and posterior axial elongation. Our findings suggest that the inductive role of FGF in mesoderm possibly predates the origin of deuterostomes.


Development ◽  
2001 ◽  
Vol 128 (2) ◽  
pp. 233-242
Author(s):  
B. San Martin ◽  
M. Bate

During Drosophila embryogenesis, the development of the midgut endoderm depends on interactions with the overlying visceral mesoderm. Here we show that the development of the hindgut also depends on cellular interactions, in this case between the inner ectoderm and outer visceral mesoderm. In this section of the gut, the ectoderm is essential for the proper specification and differentiation of the mesoderm, whereas the mesoderm is not required for the normal development of the ectoderm. Wingless and the fibroblast growth factor receptor Heartless act over sequential but interdependent phases of hindgut visceral mesoderm development. Wingless is required to establish the primordium and to enhance Heartless expression. Later, Heartless is required to promote the proper differentiation of the hindgut visceral mesoderm itself.


1998 ◽  
Vol 95 (16) ◽  
pp. 9366-9371 ◽  
Author(s):  
Maijon Park ◽  
Carol Lewis ◽  
David Turbay ◽  
Amy Chung ◽  
Jau-Nian Chen ◽  
...  

tinman, a mesodermal NK2-type homeobox gene, is absolutely required for the subdivision of the earlyDrosophilamesoderm and for the formation of the heart as well as the visceral muscle primordia. Several vertebrate relatives oftinman, many of which are predominately expressed in the very early cardiac progenitors (and pharyngeal endoderm), also seem to promote heart development. Here, we show that most of these vertebratetinman-related genes can readily substitute forDrosophila tinmanfunction in promoting visceral mesoderm-specific marker gene expression, but much less in promoting cardiac-specific gene expression indicative of heart development. In addition, another mesodermal NK2-type gene fromDrosophila,bagpipe, which is normally only needed for visceral mesoderm but not heart development, cannot substitute fortinmanat all. These data indicate that the functional equivalence of thetinman-related subclass of NK2-type genes (in activating markers of visceral mesoderm development inDrosophila) is specific to this subclass and distinct from other homeobox genes. Despite the apparent overall conservation of heart development between vertebrates and invertebrates, the differential rescue of visceral mesoderm versus heart development suggests that some of the molecular mechanisms of organ formation may have diverged during evolution.


Development ◽  
2021 ◽  
Author(s):  
Carmen Andrikou ◽  
Andreas Hejnol

FGF signaling is involved in mesoderm induction in members of deuterostomes (e.g. tunicates, hemichordates), but not in flies and nematodes, where it has a role in mesoderm patterning and migration. However, comparable studies in other protostome taxa are missing in order to decipher whether this mesoderm-inducing function of FGF extends beyond the lineage of deuterostomes. Here, we investigated the role of FGF signaling in mesoderm development in three species of lophophorates, a clade within the protostome group Spiralia. Our gene expression analyses show that the mesodermal molecular patterning is overall conserved between brachiopods and phoronids, but the spatial and temporal recruitment of transcription factors differs significantly. Moreover, the use of the inhibitor SU5402 demonstrates that FGF signaling is involved in different steps of mesoderm development, as well as in morphogenetic movements of gastrulation and axial elongation. Our findings suggest that the mesoderm-inducing role of FGF extends beyond the group of deuterostomes.


Development ◽  
1997 ◽  
Vol 124 (5) ◽  
pp. 971-982 ◽  
Author(s):  
M. Boyle ◽  
N. Bonini ◽  
S. DiNardo

The gonad forms from cells of two lineages: the germline and soma. The somatic gonadal cells generate the various cell types within the testis or ovary that support gametogenesis. These cells derive from embryonic mesoderm, but how they are specified is unknown. Here, we describe a novel regulator of Drosophila gonadogenesis, clift, mutations in which abolish gonad formation. clift is expressed within somatic gonadal precursors as these cells first form, demonstrating that 9–12 cells are selected as somatic gonadal precursors within each of three posterior parasegments at early stages in gonadogenesis. Despite this early expression, somatic gonadal precursors are specified in the absence of clift function. However, they fail to maintain their fate and, as a consequence, germ cells do not coalesce into a gonad. In addition, using clift as a marker, we show that the anteroposterior and dorsoventral position of the somatic gonadal precursor cells within a parasegment are established by the secreted growth factor Wg, coupled with a gene regulatory hierarchy within the mesoderm. While loss of wg abolishes gonadal precursors, ectopic expression expands the population such that most cells within lateral mesoderm adopt gonadal precursor fates. Initial dorsoventral positioning of somatic gonadal precursors relies on a regulatory cascade that establishes dorsal fates within the mesoderm and is subsequently refined through negative regulation by bagpipe, a gene that specifies nearby visceral mesoderm. Thus, these studies identify essential regulators of gonadal precursor specification and differentiation and reveal novel aspects of the general mechanism whereby distinct fates are allocated within the mesoderm.


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