Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation.
While the expression patterns of segment polarity genes such as engrailed have been shown to be similar in Drosophila melanogaster and Schistocerca americana (grasshopper), the expression patterns of pair-rule genes such as even-skipped are not conserved between these species. This might suggest that the factors upstream of pair-rule gene expression are not conserved across insect species. We find that, despite this, many aspects of the expression of the Drosophila gap gene hunchback are shared with its orthologs in the grasshoppers S. americana and L. migratoria. We have analyzed both mRNA and protein expression during development, and find that the grasshopper hunchback orthologs appear to have a conserved role in early axial patterning of the germ anlagen and in the specification of gnathal and thoracic primordia. In addition, distinct stepped expression levels of hunchback in the gnathal/thoracic domains suggest that grasshopper hunchback may act in a concentration-dependent fashion (as in Drosophila), although morphogenetic activity is not set up by diffusion to form a smooth gradient. Axial patterning functions appear to be performed entirely by zygotic hunchback, a fundamental difference from Drosophila in which maternal and zygotic hunchback play redundant roles. In grasshoppers, maternal hunchback activity is provided uniformly to the embryo as protein and, we suggest, serves a distinct role in distinguishing embryonic from extra-embryonic cells along the anteroposterior axis from the outset of development - a distinction made in Drosophila along the dorsoventral axis later in development. Later hunchback expression in the abdominal segments is conserved, as are patterns in the nervous system, and in both Drosophila and grasshopper, hunchback is expressed in a subset of extra-embryonic cells. Thus, while the expected domains of hunchback expression are conserved in Schistocerca, we have found surprising and fundamental differences in axial patterning, and have identified a previously unreported domain of expression in Drosophila that suggests conservation of a function in extra-embryonic patterning.
Patel
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Department of Organismal Biology and Anatomy and Howard Hughes Medical Institute, University of Chicago, 5841 S. Maryland Ave., MC1028, Chicago, IL 60637, USA. npatel@midway.uchicago.edu
Hayward
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DC
Lall
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Pirkl
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DiPietro
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Ball
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D000595:Amino Acid Sequence; D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning; D003001:Cloning, Molecular; D017124:Conserved Sequence; D004268:DNA-Binding Proteins / Q000235:genetics / Q000302:isolation & purification*; D029721:Drosophila Proteins; D005854:Germ Cells; D006110:Grasshoppers / Q000196:embryology* / Q000235:genetics; D017403:In Situ Hybridization; D008648:Mesoderm; D008969:Molecular Sequence Data; D009420:Nervous System; D009866:Oogenesis; D017422:Sequence Analysis, DNA; D017386:Sequence Homology, Amino Acid; D014018:Tissue Distribution; D014157:Transcription Factors / Q000235:genetics / Q000302:isolation & purification*; D016335:Zinc Fingers / Q000235:genetics
D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D014157:Transcription Factors; C061245:hb protein, Drosophila