Analysis of Biological Development (K. Kalthoff)

Updates to Topic 22G: Patterning Genes in Other Insects

New Review Articles

Grbic M. (2000) "Alien" wasps and evolution of development. Bioessays 22: 920-932

New Research Articles

Grbic M., Nagy L.M., Carroll S.B., and Strand M. (1996) Polyembryonic development: insect pattern formation in a cellularized environment. Development 122: 795-804

The egg of the parasitic wasp Copidosoma floridanum is exceptional in having holoblastic cleavage and giving rise to about 2,000 embryos, each embryo consisting initially of about 20 cells. Nevertheless, immunostaining with antibodies against evenskipped (eve), engrailed, and Ultrabithorax/Abdominal A revealed the same distributions of these proteins as they are known from Drosophila, except that eve accumulates in 15 stripes of segmental periodicity. These protein distributions must originate without a syncytial blastoderm stage during which transcription factors encoded by patterning genes can diffuse without barriers as they do in Drosophila. An interpretation of these unexpected results will have to await studies on those Hymenopterans with superficial cleavage from which Copidosoma evolved.

Hughes C.L. and Kaufman T.C. (2000) RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 127: 3683-3694

The investigators used a new methodology, RNA interference (RNAi), to mimic the effects of mutations in the Hox genes known from genetic analyses of the fruit fly Drosophila melanogaster and the flour beetle Tribolium castaneum. RNAi involves the injection of double-stranded RNA of the same sequence as the relevant mRNA resulting in a depletion of that transcript. The study is focused on the gnathal segments of the milkweed bug, Oncopeltus fasciatus, which has specialized suctorial mouthparts. The Hox genes Deformed+ (Dfd+), proboscipedia+ (pb+) and Sex combs reduced+ (Scr+) have previously been shown to be expressed in the gnathal appendages of this species. The exact roles of the genes, however, are different from what is known in the two genetic model insects. The maxillary appendages in the bug are determined by the activities of the genes Dfd+ and Scr+, rather than Dfd+ and pb+ as in the fly and beetle. The mandibular appendages are specified by Dfd+, but their unique morphology in Oncopeltus suggests that Dfd's target genes are different. As in flies and beetles, the labium is specified by the combined activities of pb+ and Scr+, but again, the function of pb+ appears to be different. Additionally, the regulatory control of pb+ by the other two genes seems to be different in the bug than in either of the other species. These novelties in Hox function, expression pattern and regulatory relationships may have been important for the evolution of the unique Hemipteran head.

Hughes CL, Kaufman TC. (2002) Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol. 247: 47-61.

Hughes CL, Kaufman TC. (2002) Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. Development 129: 1225-1238.

The investigators used in situ hybridization to analyze the expression patterns of three segmentation genes (even-skipped, engrailed, and wingless) and ten Hox genes in a centipede, Lithobius atkinsoni. The expression of the segmentation genes in the centipede suggests that their basic roles are conserved across the mandibulate arthropods. For example, unlike the seven pair-rule stripes of eve expression in the Drosophila embryonic germband, the centipede eve gene is expressed strongly in the posterior of the embryo, and in only a few stripes between newly formed segments. Nonetheless, this pattern likely reflects a conserved role for eve in the process of segment formation, within the different context of a short-germband mode of embryonic development. In the centipede, the genes wingless and engrailed are expressed in stripes along the middle and posterior of each segment, respectively, similar to their expression in Drosophila. The adjacent expression of the engrailed and wingless stripes suggests that the regulatory relationship between the two genes may be conserved in the centipede, and thus this pathway may be a fundamental mechanism of segmental development in most arthropods.

With regard to the Hox genes, the researchers report three major findings. First, that the expression patterns in the centipede are in many cases intermediate between those of the chelicerates (horse shoe crabs, spiders, and scorpions) and those of the insects and crustaceans (lobsters, shrimps, etc.). This result is consistent with the proposed intermediate phylogenetic position of the centipeds. Second, we found two 'extra' Hox genes in the centipede compared with those in Drosophila. Based on its pattern of expression, Hox3 appears to have a typical Hox-like role in the centipede, suggesting that the novel functions of the Hox3 homologs zen and bicoid were adopted somewhere in the crustacean-insect clade. In the centipede, the expression of the gene fushi tarazu suggests that it has both a Hox-like role (as in the mite), as well as a role in segmentation (as in insects). This suggests that this dramatic change in function was achieved via a multifunctional intermediate, a condition maintained in the centipede. Last, Hox expression correlates with boundaries between major body regions (such as head, thorax, and abdomen in insects), consistent with the theory that changes in Hox genes had a major role in evolution of the arthropod body plan.

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