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First published online 24 November 2004
doi: 10.1242/dev.01561

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Functional analyses of tiptop and Antennapedia in the embryonic development of Oncopeltus fasciatus suggests an evolutionary pathway from ground state to insect legs

Louisiana State University, Department of Biological Sciences, Baton Rouge, LA 70803, USA Department of Biological Sciences, 202 Life Sciences Building, Louisiana State University, Baton Rouge, LA 70803, USA

View larger version (66K): [in a new window]   Fig. 7. Model of leg specification mechanisms in D. melanogaster and O. fasciatus, an O. fasciatus leg divided into proximal, medial and distal regions. The D. melanogaster mechanism is shown on the left and correlates required gene activities with the regions of the leg. A proposed tiptop-like activity (tiptop?) is required for the segmentation and identity of distal segments and the pretarsus. Antp limits the distal extent of hth activity, is required for medial segmentation, and specifies distal, medial and proximal segment identities. hth is required for medial and proximal segmentation. Differences in the O. fasciatus mechanism are shown on the right. tiptop, but not Antp, limits the distal extent of the antennal specifier (hth?) activity. Antp is required for distal and medial segmentation, but does not affect proximal identity. tsh is not required for proximal identities or segmentation.

View larger version (16K): [in a new window]   Fig. 1. Alignment of partial tsh-like proteins from insects. Portions of the conceptual proteins translated from cDNA sequence are aligned to show that insect tsh-family members have greater similarity to tiptop than to tsh. In this alignment, dashes represent amino acids identical to the tsh residues at that position. For orientation, the position of the second zinc finger and the consensus sequence for tsh zinc fingers are also shown. Dots represent any amino acid. DM: D. melanogaster, TD: T. domestica, OF: O. fasciatus, CF: Ctenocephalides felis, TC: T. castaneum. For complete clone sequences, see the tiptop GenBank Accession Numbers: Of: AF533539, Tc: AF356647, Td: AF104011, Cf: AF533538, Dm: AF219383, Dm tsh: M57496.

View larger version (104K): [in a new window]   Fig. 2. The embryonic accumulation of tiptop mRNA is revealed by in situ hybridization. (A) mRNA accumulation is first detected in the thoracic (T), labial (Lb) and maxillary (Mx) segments of the elongating germband and is highest in the thorax. During germband extension (B), mRNA can be detected in the procephalon (D) including the labral (Lr), antennal (An) and ocular (Oc) segments. (C) At the fully extended germband stage, mRNA accumulates in the caudal (cad) region and weakly in the first abdominal (A1) and mandibular (Mn) segments. The darkening of the posterior abdomen in this animal results from nonspecific chromogen and unremoved yolk; it does not represent tiptop expression. (E) After germband extension, mRNA accumulation becomes mosaic in the legs. Anterior arcs of elevated accumulation (small arrows) form and regions of the distal tips lose expression completely (large arrow). Ic: intercalary segment.

View larger version (81K): [in a new window]   Fig. 3. tiptop RNA-I causes a range of embryonic defects that only affect the leg. (A) Control injections produce normal morphology. (B) Moderate tiptop phenocopies show segmentation abnormalities in the distal leg. (C) Strong tiptop phenocopies show distal legs transformed to antennae. Distal legs are marked with a white arrow. All other regions of the animals appeared normal based on general morphology and the presence of cuticular structures such as bristles, sense organs, and spiracles.

View larger version (133K): [in a new window]   Fig. 4. The moderate tiptop phenocopy shows a loss of pretarsi and reduction of tarsi (C,D). (A) A leg of a buffer-injected animal displaying a normal phenotype. (B) Detail of the pretarsus in (A), the arrow marks the tarsus-tibia junction in A,C,D. Fe: femur, Ti: tibia, Ta: tarsus.

View larger version (182K): [in a new window]   Fig. 5. The strong tiptop phenocopy displays a transformation of distal leg to antennae. (A) A normal antenna. (B) Close up of (A) showing antennal-specific sensory pegs (arrow). (C-F) Legs displaying the strong phenocopy. Tarsi and pretarsi are absent. The presumptive tibia (Ti) is the most distal segment and is transformed toward antenna based on its shape, a bristle density gradient and the presence of the antennal-specific sensory pegs (arrows in E,F). Fe: femur.

View larger version (89K): [in a new window]   Fig. 6. Antp and tiptop are required for distal and medial development. (A) The weak Antp phenocopy has an apparent fusion of medial segments (M*=Fe+Ti). (B) The strong Antp phenocopy has a fusion of medial and distal (DM*=Fe+Ti+Ta). (C) The strong tiptop phenocopy has a fusion of distal segments (D*=Ti+Ta) and D* has an antennal identity. The femur is shortened in some animals, but is otherwise normal. (D) In the strong Antp tiptop phenocopy, DM* has an antennal identity. All appendages have normal coxa (Cx) and trochanter (Tr) that can be identified by unique sense organ clusters (arrows in A,B,D) found at the proximal edges of the segments. Pt: pretarsus.