The T-box-encoding Dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp

Reim, Ingolf; Lee, Hsiu‐Hsiang; Frasch, Manfred

doi:10.1242/dev.00548

Cited by 123 publications

(174 citation statements)

References 64 publications

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“…C15 null mutations do not interfere with larval hatching, indicating that their amnioserosa is essentially intact (35). Doc-and Tup-deficient embryos exhibit defects in the maintenance of amnioserosa cells only after stage 8 (25,36). Thus, doc and tup unfold their function in the amnioserosa, with one exception (see below), after zen expression has been suppressed.…”

Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

“…Genetic changes upstream of zen must have occurred in the Drosophila lineage to allow these changes in zen expression and function (31). In addition, genetic changes immediately downstream of zen must have occurred to allow the coexpression of ''serosa genes'' (zen and Kr) together with C15, pnr, dorsoccross (doc), and tail-up (tup) (25,32,33), which have been described as amnion markers in other species (14, 31) (Fig. 4).…”

Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

“…Our model implies that these functions of doc and tup are comparable to the function of their homologues in the amnion of lower Diptera. The amnioserosa of Doc-deficient embryos also fails to fold properly during germband extension, whereas zen is still expressed (25). This phenotype of a putative ''amnion gene'' in the early amnioserosa could suggest that some amnion properties of the amnioserosa unfold before zen expression is down-regulated.…”

Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

“…In Drosophila, the transcripts and proteins of all three genes are expressed throughout the developing amnioserosa, albeit in different time windows. Extraembryonic C15 expression starts in the blastoderm and continues until after germband retraction (25,26). Extraembryonic pnr expression starts in the blastoderm and fades during the extended germband stage (stage 10) (27).…”

Section: Phenotypic Effects Of Zen Rnai In Megaselia and Episyrphusmentioning

confidence: 99%

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Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

Rafiqi

Lemke

Ferguson

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

121

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Higher cyclorrhaphan flies including Drosophila develop a single extraembryonic epithelium (amnioserosa), which closes the germband dorsally. In most other insects two extraembryonic epithelia, serosa and amnion, line the inner eggshell and the ventral germband, respectively. How the two extraembryonic epithelia evolved into one is unclear. Recent studies have shown that, in the flour beetle Tribolium and in the milkweed bug Oncopeltus, the homeobox gene zerknü llt (zen) controls the fusion of the amnion with the serosa before dorsal closure. To understand the origin of the amnioserosa in evolution, we examined the expression and function of zen in the extraembryonic tissue of lower Cyclorrhapha. We show that Megaselia abdita (Phoridae) and Episyrphus balteatus (Syrphidae) develop a serosa and a dorsal amnion, suggesting that a dorsal amnion preceded the origin of the amnioserosa in evolution. Using Krü ppel (Kr) and pannier (pnr) homologues of Megaselia as markers for serosal and amniotic tissue, respectively, we show that after zen RNAi all extraembryonic tissue becomes indistinguishable from amniotic cells, like in Tribolium but unlike in Drosophila, in which zen controls all aspects of extraembryonic development. Compared with Megaselia and Episyrphus, zen expression in Drosophila is extended to cells that form the amnion in lower Cyclorrhapha and is down-regulated at the developmental stage, when serosa cells in lower Cyclorrhapha begin to expand. These expression differences between species with distinct extraembryonic tissue organizations and the conserved requirement of zen for serosa development suggest that the origin of an amnioserosa-like epithelium was accompanied by expression changes of zen.Megaselia ͉ Episyrphus ͉ Drosophila ͉ EvoDevo ͉ homology

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Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

Section: Discussion Two Major Transitions In Extraembryonic Morphologmentioning

confidence: 99%

Section: Phenotypic Effects Of Zen Rnai In Megaselia and Episyrphusmentioning

confidence: 99%

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Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

Rafiqi

Lemke

Ferguson

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

121

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“…The Tbx6 subfamily is composed of Dorsocross 1, 2, and 3, which are expressed in identical patterns and play redundant roles in the amnioserosa, heart, and hindgut. These proteins are key components in cardiogenesis and are required for formation of most myocardial and pericardial cells (Reim et al 2003;Hamaguchi et al 2004;Hamaguchi et al 2012). Brachyenteron, the ortholog of vertebrate Brachyury, mediates the early specification of the caudal visceral mesoderm (Kusch and Reuter 1999;Hamaguchi et al 2012).…”

Section: Mid and The T-box Family Of Proteinsmentioning

confidence: 99%

Muscle Cell Fate Choice Requires the T-Box Transcription Factor Midline in Drosophila

et al. 2015

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Drosophila Midline (Mid) is an ortholog of vertebrate Tbx20, which plays roles in the developing heart, migrating cranial motor neurons, and endothelial cells. Mid functions in cell-fate specification and differentiation of tissues that include the ectoderm, cardioblasts, neuroblasts, and egg chambers; however, a role in the somatic musculature has not been described. We identified mid in genetic and molecular screens for factors contributing to somatic muscle morphogenesis. Mid is expressed in founder cells (FCs) for several muscle fibers, and functions cooperatively with the T-box protein H15 in lateral oblique muscle 1 and the segment border muscle. Mid is particularly important for the specification and development of the lateral transverse (LT) muscles LT3 and LT4, which arise by asymmetric division of a single muscle progenitor. Mid is expressed in this progenitor and its two sibling FCs, but is maintained only in the LT4 FC. Both muscles were frequently missing in mid mutant embryos, and LT4-associated expression of the transcription factor Krüppel (Kr) was lost. When present, LT4 adopted an LT3-like morphology. Coordinately, mid misexpression caused LT3 to adopt an LT4-like morphology and was associated with ectopic Kr expression. From these data, we concluded that mid functions first in the progenitor to direct development of LT3 and LT4, and later in the FCs to influence whichever of these differentiation profiles is selected. Mid is the first T-box factor shown to influence LT3 and LT4 muscle identity and, along with the T-box protein Optomotor-blind-related-gene 1 (Org-1), is representative of a new class of transcription factors in muscle specification. KEYWORDS midline; Tbx20; founder cell; muscle identity; differentiation T HE body wall muscles of the Drosophila larva are composed of a stereotypic pattern that includes 30 unique muscle fibers (each a single myotube) per abdominal hemisegment (Bate 1990). These muscles form during embryogenesis, during which time they take on unique characteristics such as size, shape, pattern of innervation, and epidermal attachment Baylies et al. 1998;Frasch 1999;De Joussineau et al. 2012). The unique identity of each muscle fiber is conferred through overlapping signaling pathways and cell autonomous transcription factors that specify muscle progenitors Baylies et al. 1998;Frasch 1999;Tixier et al. 2010), which then undergo asymmetric cell division to generate founder cells (FCs) (Bate 1990;Carmena et al. 1998). A single FC initiates the formation of multinucleate syncytia by fusing with fusion competent myoblasts (FCMs) (Rochlin et al. 2010;Abmayr and Pavlath 2012). FCs dictate the number of cell fusion events that take place, leading to a characteristic number of nuclei for each muscle in the pattern . These fusing nuclei adopt the transcriptional profile of the original FC nucleus (Bourgouin et al. 1992;D'Alessio and Frasch 1996;Ruiz-Gomez et al. 1997;Jagla et al. 1998;Keller et al. 1998;Nose et al. 1998;Crozatier and Vincent 1999;Knirr et al. 1999;D...

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T‐box genes and heart development: Putting the “T” in heart

Plageman

Yutzey

2004

Developmental Dynamics

155

116

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Members of the T-box gene family (Tbx) are essential for normal heart development, and mutations in human TBX genes cause congenital cardiovascular malformations. T-box genes have been implicated in early cardiac lineage determination, chamber specification, valvuloseptal development, and diversification of the specialized conduction system in vertebrate embryos. These genes include Tbx1, Tbx2, Tbx3, Tbx5, Tbx18, and Tbx20, all of which exhibit complex temporal spatial regulation in developing cardiac structures. Less is known about T-box genes in invertebrate heart development, but multiple T-box genes are expressed in Drosophila cardiac lineages. The molecular hierarchies and developmental processes controlled by T-box genes in the heart are the focus of this review. Developmental Dynamics 232:11-20, 2005.

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The T-box-encoding Dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp

Cited by 123 publications

References 64 publications

Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

Muscle Cell Fate Choice Requires the T-Box Transcription Factor Midline in Drosophila

T‐box genes and heart development: Putting the “T” in heart

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