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Segmentation and Specification of the Drosophila Mesoderm

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Segmentation and Specification of the Drosophila Mesoderm Downloaded from genesdev.cshlp.org on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Segmentation and specification of the Drosophila mesoderm Natalia Azpiazu, 1,3 Peter A. Lawrence, 2 Jean-Paul Vincent, 2 and Manfred Frasch 1'4 1Brookdale Center for Molecular Biology, Mount Sinai School of Medicine, New York, New York 10029 USA; 2Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 2QH, UK Patterning of the developing mesoderm establishes primordia of the visceral, somatic, and cardiac tissues at defined anteroposterior and dorsoventral positions in each segment. Here we examine the mechanisms that locate and determine these primordia. We focus on the regulation of two mesodermal genes: bagpipe (hap), which defines the anlagen of the visceral musculature of the midgut, and serpent (srp), which marks the anlagen of the fat body. These two genes are activated in specific groups of mesodermal cells in the anterior portions of each parasegment. Other genes mark the anlagen of the cardiac and somatic mesoderm and these are expressed mainly in cells derived from posterior portions of each parasegment. Thus the parasegments appear to be subdivided, at least with respect to these genes, a subdivision that depends on pair-rule genes such as even-skipped (eve). We show with genetic mosaics that eve acts autonomously within the mesoderm. We also show that hedgehog (hh) and wingless (wg) mediate pair-rule gene functions in the mesoderm, probably partly by acting within the mesoderm and partly by inductive signaling from the ectoderm, hh is required for the normal activation of hap and srp in anterior portions of each parasegment, whereas wg is required to suppress bap and srp expression in posterior portions. Hence, hh and wg play opposing roles in mesoderm segmentation. [Key Words: Mesoderm; segmentation; visceral musculature; fat body; heart; even-skipped; wingless; hedgehog] Received September 4, 1996; revised version accepted November 1, 1996. How does the Drosophila mesoderm become subdivided dermal areas (Azpiazu and Frasch 1993; Staehling-Hamp- into different anlagen? The mesoderm is partitioned ton et al. 1994). bap is involved in the determination of along the dorsoventral axis: dorsally, cells found the pri- the anlagen of the midgut visceral mesoderm. Analogous mordia of the cardiac and visceral mesoderm and this events could activate tin target genes that would specify subdivision is triggered by inductive inputs from the ec- the anlagen of the heart and dorsal body wall muscula- toderm. Dpp is a TGF~ protein that is secreted from ture. dorsal ectodermal cells, and has been identified as the We now study patterning of the mesoderm along the inductive signal (Staehling-Hampton et al. 1994; Frasch anteroposterior axis of the embryo. The morphology of 1995). Dpp signaling is required for the formation of the the early mesoderm and the spatial domains of expres- anlagen of the heart and the midgut visceral mesoderm, sion of homeotic genes indicate that the mesoderm is and the dorsoventral extent of the visceral mesoderm is organized into parasegmental units (for review, see directly determined by the dorsoventral limits of dpp Lawrence 1992). Previous attempts to identify distinct expression in the ectoderm (Frasch 1995; Maggert et al. subdivisions within each mesodermal parasegment that 1995). An early response to the Dpp signal in mesoder- might be homologous to the anterior and posterior com- mal cells is the spatial restriction of expression of the partments of the ectoderm were negative (Lawrence and homeo-box gene tinman (tin) to dorsal portions of the Johnston 1984). However, more recently, the analysis of mesoderm, tin provides the dorsal mesoderm with the expression patterns of genes that control mesoderm de- competence to form midgut visceral mesoderm, dorsal velopment has suggested that mesodermal parasegments muscles, and the heart (Azpiazu and Frasch 1993; Bod- are indeed subdivided into anterior and posterior por- mer 1993). In combination with additional regulators tions with different developmental fates. A clear exam- that may include Dpp, tin activates the expression of a ple is the expression of the homeo-box gene bap which is second homeo-box gene, bagpipe (bap), in dorsal meso- restricted to metameric clusters of cells in the dorsal mesoderm (Azpiazu and Frasch 1993). Under the control of bap, these cell clusters develop into midgut visceral mesoderm, whereas cells in segmental portions lacking 3Present address: Centro de Biologia Molecular "Severo Ochoa," Facul- tad de Ciencias, Universita Autonoma de Madrid, Madrid 28034, Spain. bap expression form other mesodermal derivatives. The 4Corresponding author. expression of several marker genes in the anlagen of the GENES & DEVELOPMENT 10:3183-3194 91996 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/96 $5.00 3183 Downloaded from genesdev.cshlp.org on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Azpiazu et al. fat body and studies on the regulatory gene twist also (Fig. 1D) show that these cells are at the same antero- indicate that cells at different anteroposterior positions posterior positions and lie just ventrolateral to the pri- within each mesodermal parasegment give rise to differ- mordia of the midgut visceral mesoderm. ent mesodermal derivatives (Abel et al. 1993; Hoshizaki In summary, the mesoderm of stage 10-11 embryos et al. 1994; Dunin-Borkowski et al. 1995; Baylies and appears to be organized into parasegmental repeats that Bate 1996). are in exact register with the ectodermal parasegments. By analogy to dorsoventral patterning, inductive sig- Each parasegment is subdivided into two domains along nals from the segmented ectoderm could help segment the anteroposterior axis. In keeping with the nomencla- the mesoderm. Alternatively, the mesoderm could seg- ture used for the ectoderm (Lawrence 1992), we term the ment itself autonomously. For example, wingless (wg) mesodermal domains below the anterior compartments acts in heart and muscle development and can function "A domains" and those below the posterior compart- either from within the ectoderm or from the mesoderm ments "P domains." As shown schematically in Figure (Baylies et al. 1995; Lawrence et al. 1995; Wu et al. 1995; 1E, the P domains express bap and srp and give rise to Ranganayakulu et al. 1996). However, there must be ad- visceral mesoderm derivatives that include midgut mus- ditional segmental regulators, because both in the ab- culature and the fat body. The A domains include the sence of wg and in the presence of uniformly distributed primordia of the cardiac mesoderm and the bulk of the Wg protein the mesoderm is still segmentally patterned. somatic mesoderm and give rise to the heart and most of Our experiments show that the mesoderm forms seg- the body wall muscles. ments autonomously, although induction from the ecto- derm also contributes. We show that wg and hedgehog (hh), which are candidates for inductive signals from the A mesoderm-autonomous role of pair rule genes in ectoderm, play opposite and antagonistic roles in the segmentation and specification of the visceral subdivision of mesodermal parasegments, wg is mainly mesoderm involved in the formation of derivatives from posterior portions of each parasegment, including somatic muscu- The close alignment between mesodermal and ectoder- lature and the heart, whereas hh functions mainly in the mal parasegments suggests that the two germ layers formation of derivatives in anterior parasegmental por- might be segmented by the same genes. Indeed, muta- tions, in particular the visceral mesoderm of the midgut tions in pair rule genes have similar effects in both the musculature and the fat body. ectoderm and the mesoderm. For example, fushi tarazu (ftz) mutant embryos retain only six out of normally 13 en stripes between parasegments 2 and 14 in wild-type embryos, and the number of bap patches is similarly Results reduced from normally 11 to 5 (Fig. 2A; note that para- segments 13 and 14 lack bap expression even in wild- Segmental organization of mesodermal primordia type embryos; see Fig. 1A). srp patches are also reduced The expression patterns of several genes reveal that the in ftz mutant embryos (Fig. 2B; wild-type expression early mesoderm is segmented. Notably, the homeo-box only occurs between parasegments 4 and 12; see Fig. 1C). gene bap is expressed in 11 metameric clusters of dorsal In spite of their aberrant patterns, the normal spatial mesodermal cells that develop into visceral musculature relationships between the bap or srp domains and the en of the midgut (Azpiazu and Frasch 1993). The anterior stripes are maintained in ftz mutants, indicating that ftz borders of each of the bap patches coincide with the mutations cause identical alterations in the mesoderm parasegmental borders of the ectoderm--thus the pri- and ectoderm. Concomitant alterations of bap and en mordia of the midgut visceral mesoderm are largely po- stripes are observed in mutants for all other pair-rule sitioned below the posterior compartments of the ecto- genes tested, including hairy (h; Fig. 2C), runt (run; Fig. derm (Fig. 1A; Azpiazu and Frasch 1993). The homeo-box 2D), paired (prd; Fig. 2E), odd-paired (opa; Fig. 2F), and gene even-skipped (eve) marks heart progenitors that odd-skipped (odd; data not shown). Pair-rule mutations will form pericardial cells (Frasch et al. 1987). Double that cause mirror-image arrangements in the ectoderm, stainings for bap and eve demonstrate that these heart such as runt (Nhsslein-Volhard and Wieschaus 1980), re- progenitors form between the bap patches at the dorsal sult in mirror-image arrangements of the bap patches in crest of the mesoderm (Fig. 1B). In addition, the progen- the mesoderm (Fig. 2D). itors of the cardioblasts are formed in close juxtaposi- The importance of pair-rule genes to segmentation of tion, just anterior to the pericardial progenitors (K. Jagla, the mesoderm is particularly obvious in embryos that pets. comm.). Thus, it appears that the anlagen of the are mutant for eve.
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