Maternal Torso Signaling Controls Body Axis Elongation in a Short Germ Insect

Abstract

In the long germ insect Drosophila, all body segments are determined almost simultaneously at the blastoderm stage under the control of the anterior, the posterior, and the terminal genetic system . Most other arthropods (and similarly also vertebrates) develop more slowly as short germ embryos, where only the anterior body segments are specified early in embryogenesis. The body axis extends later by the sequential addition of new segments from the growth zone or the tail bud . The mechanisms that initiate or maintain the elongation of the body axis (axial growth) are poorly understood . We functionally analyzed the terminal system in the short germ insect Tribolium. Unexpectedly, Torso signaling is required for setting up or maintaining a functional growth zone and at the anterior for the extraembryonic serosa. Thus, as in Drosophila, fates at both poles of the blastoderm embryo depend on terminal genes, but different tissues are patterned in Tribolium. Short germ development as seen in Tribolium likely represents the ancestral mode of how the primary body axis is set up during embryogenesis. We therefore conclude that the ancient function of the terminal system mainly was to define a growth zone and that in phylogenetically derived insects like Drosophila, Torso signaling became restricted to the determination of terminal body structures.

Apparent role of Tribolium orthodenticle in anteroposterior blastoderm patterning largely reflects novel functions in dorsoventral axis formation and cell survival

“…4), it is unlikely that the Tc-zen-1 expression boundary is read from the Tc-Otd-1 gradient as, at this anterior position in the egg, Tc-Otd-1 expression levels are rather uniform throughout blastoderm development (Schroder, 2003). Instead, the terminal system appears to provide a short-range graded signal near the anterior pole, which is enhanced by Tc-Otd-1 (Schoppmeier and Schroder, 2005).…”

“…2). In wild-type embryos, Tc-eve is initially expressed in a double-segmental pattern, each stripe later resolving into secondary segmental stripes (Patel et al, 1994;Schoppmeier and Schroder, 2005). The first two primary Tc-eve stripes (Tc-eve stripe 1 and stripe 2; Fig.…”

“…Development 137 (11) prominent role in early axis formation (Schoppmeier and Schroder, 2005). At the posterior, Torso-signaling is required for growth zone formation and, at the anterior, it is involved in serosa formation via activation of Tc-zen-1 (Fig.…”

Maternal activation of gap genes in the hover flyEpisyrphus

“…A single primer pair was used to isolate Episyrphus orthologs of knirps and knirps-related (Eba-kni and Eba-knrl; 5Ј-CCGGCRGCNGGNTTYCAYTTYGG and 5Ј-ARRCARTGRATY -TTRAACCARTTNGA), huckebein (Eba-hkb; 5Ј-CARACVTAYTC R -CGNYTNTTCCG and 5Ј-CGYTCYWKNGGCAWRTGMGTYTT) and tailless (Eba-tll) (Schröder et al, 2000). Two primer pairs were used in a nested PCR for the isolation of Episyrphus orthologs of Krüppel (Eba-Kr) , giant [Eba-gt; 5Ј-TTCAARGCNTWYCCN -MRNGAYCC and 5Ј-GCCCKRATNGCNATYTCRTCYTCYT; nested 5Ј-GARMGNMGNMGNAARAAYAA (Bucher and Klingler, 2004) and 5Ј-GCCCKRATNGCNATYTCRTCYTCYT] and torso [Eba-tor; 5Ј-GTNCAYMGNGAYYTNGCNGC (Schoppmeier and Schröder, 2005) and 5Ј-TKCCNCCKAGNGTKNNKATCTC; nested 5Ј-TNYCMGAYTT Y -GGNCTNAGTCGNGA and 5Ј-ARNAYNCCRAANSWCCANACRTC (Schoppmeier and Schröder, 2005)]. A homolog of bicoid (Eba-bcd) was identified in 454 transcriptome sequences of normalized cDNA from 0-to 4-hour-old Episyrphus embryos.…”

Two distinct but convergent groups of cells trigger Torso receptor tyrosine kinase activation by independently expressing torso-like

“…26). In Tribolium, an insect with a more primitive ovary in which tsl expression has been examined, tsl is precisely expressed in the follicle cells overlying both edges of the oocyte (27). Therefore, Drosophila tsl expression in the BCs and PFCs may represent an adaptation, or the remnant, of a more ancient pattern of tsl expression.…”