Homeotic genes and the arthropod head: Expression patterns of the labial, proboscipedia, and Deformed genes in crustaceans and insects

Department of Biology, Indiana University Bloomington, Bloomington, Indiana, United States
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/1999; 96(18):10224-9. DOI: 10.1073/pnas.96.18.10224
Source: PubMed


cDNA fragments of the homologues of the Drosophila head homeotic genes labial (lab), proboscipedia (pb), and Deformed (Dfd) have been isolated from the crustacean Porcellio scaber. Because the accumulation domains of the head homeotic complex (Hox) genes had not been previously reported for crustaceans, we studied the expression patterns of these genes in P. scaber embryos by using in situ hybridization. The P. scaber lab homologue is expressed in the developing second antennal segment and its appendages. This expression domain in crustaceans and in the homologous intercalary segment of insects suggests that the lab gene specified this metamere in the last common ancestor of these two groups. The expression domain of the P. scaber pb gene is in the posterior part of the second antennal segment. This domain, in contrast to that in insects, is colinear with the domains of other head genes in P. scaber, and it differs from the insect pb gene expression domain in the posterior mouthparts, suggesting that the insect and crustacean patterns evolved independently from a broader ancestral domain similar to that found in modern chelicerates. P. scaber Dfd is expressed in the mandibular segment and paragnaths (a pair of ventral mouthpart structures associated with the stomodeum) and differs from insects, where expression is in the mandibular and maxillary segments. Thus, like pb, Dfd shows a divergent Hox gene deployment. We conclude that homologous structures of the mandibulate head display striking differences in their underlying developmental programs related to Hox gene expression.

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Available from: Arhat Abzhanov,
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    • "Collinear patterns of Hox genes expression are controlled by multiple proximal regulatory elements scattered throughout the clusters (Spitz et al., 2001; T€ umpel et al., 2009). Similar to Drosophila, the transcription of the most anterior Hox genes, members of paralog groups 1–4, is restricted to one or two segments of the developing hindbrain (Abzhanov and Kaufman, 1999; T€ umpel et al., 2009). In contrast, in more posterior structures like the spinal cord, Hox genes are expressed in large overlapping domains (Carpenter, 2002). "
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    ABSTRACT: Hox genes encode transcription factors defining cellular identities along the major and secondary body axes. Their coordinated expression in both space and time is critical for embryonic patterning. Accordingly, Hox genes transcription is tightly controlled at multiple levels, and involves an intricate combination of local and long-range cis-regulatory elements. Recent studies revealed that in addition to transcription factors, dynamic patterns of histone marks and higher-order chromatin structure are important determinants of Hox gene regulation. Furthermore, the emerging picture suggests an involvement of various species of non-coding RNA in targeting activating and repressive complexes to Hox clusters. I review these recent developments and discuss their relevance to the control of Hox gene expression in vivo, as well as to our understanding of transcriptional regulatory mechanisms. Developmental Dynamics, 2013. © 2013 Wiley Periodicals, Inc.
    Developmental Dynamics 01/2014; 243(1). DOI:10.1002/dvdy.24014 · 2.38 Impact Factor
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    • "Dfd is expressed in the mandible and maxilla bearing segments in the majority of mandibulates and expression is stronger in the protopodite than in the palps of maxillary appendages [36,39,62-66]. There is loss of Dfd expression in the mandibular limb bud across mandibulates, as in Tribolium and Drosophila[24,35,65,66]. Expression of pb is conserved in the telopodites of these maxillary appendages [39,65,67]. "
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    ABSTRACT: Background The biting mandible of the arthropods is thought to have evolved in the ancestor of the insects, crustaceans and myriapods: the Mandibulata. A unique origin suggests a common set of developmental genes will be required to pattern the mandible in different arthropods. To date we have functional studies on patterning of the mandibular segment of Drosophila melanogaster showing in particular the effects of the gene cap’n’collar (cnc), however, the dipteran head is far from representative of insects or of more distantly related mandibulates; Drosophila does not even possess a mandibular appendage. To study the development of a more representative insect mandible, we chose the red flour beetle Tribolium castaneum and investigated the function of the Tribolium orthologs of cap’n’collar (Tc-cnc) and the Hox gene Deformed (Tc-Dfd). In order to determine the function of Tc-cnc and Tc-Dfd, transcripts were knocked down by maternal RNA interference (RNAi). The effects of gene knockdown were examined in the developing embryos and larvae. The effect of Tc-cnc and Tc-Dfd knockdown on the expression of other genes was determined by using in situ hybridization on Tribolium embryos. Results Our analyses show that Tc-cnc is required for specification of the identity of the mandibular segment of Tribolium and differentiates the mandible from maxillary identity. Loss of Tc-cnc function results in a transformation of the mandible to maxillary identity as well as deletion of the labrum. Tc-Dfd and the Tribolium homolog of proboscipedia (Tc-mxp = maxillopedia), Hox genes that are required to pattern the maxillary appendage, are expressed in a maxilla-like manner in the transformed mandible. Tribolium homologs of paired (Tc-prd) and Distal-less (Tc-Dll) that are expressed in the endites and telopodites of embryonic appendages are also expressed in a maxilla-like manner in the transformed mandible. We also show that Tc-Dfd is required to activate the collar of Tc-cnc expression in the mandibular segment but not the cap expression in the labrum. Tc-Dfd is also required for the activation of Tc-prd in the endites of the mandible and maxillary appendages. Conclusions Tc-cnc is necessary for patterning the mandibular segment of Tribolium. Together, Tc-cnc and Tc-Dfd cooperate to specify mandibular identity, as in Drosophila. Expression patterns of the homologs of cnc and Dfd are conserved in mandibulate arthropods suggesting that the mandible specifying function of cnc is likely to be conserved across the mandibulate arthropods.
    EvoDevo 11/2012; 3(1):25. DOI:10.1186/2041-9139-3-25 · 3.03 Impact Factor
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    • "These data suggest a correlation between the anterior boundaries of the posteriormost three Hox genes and the fate of the opisthosomal segments they pattern. Evolution of the anterior boundary of Ubx has been examined in several other chelicerates, including a xiphosuran, a scorpion, and three spiders (Damen et al. 1998; Abzhanov et al. 1999; Popadic and Nagy 2001). Together with these data, the expression domain of Po-Ubx corroborates the observation that, in contrast to crustaceans, changes in the embryonic expression of Ubx are not correlated with changes in adult morphology of chelicerates (Popadic and Nagy 2001). "
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    ABSTRACT: Among chelicerates, Hox gene expression has only been investigated in representatives of two arachnid orders to date: Acari (mites and ticks) and Araneae (spiders). Limited data are available for the "primitive" arachnid orders, such as Scorpiones (scorpions) and Opiliones (harvestmen). Here, we present the first data on Hox gene expression in the harvestman Phalangium opilio. Ten Hox genes of this species were obtained from a de novo assembled developmental transcriptome using the Illumina GAII platform. All 10 genes are expressed in characteristic Hox-like expression patterns, and the expression of the anterior and central Hox genes is similar to those of other chelicerates. However, intriguingly, the three posteriormost genes-Ultrabithorax, abdominal-A, and Abdominal-B-share an identical anterior expression boundary in the second opisthosomal segment, and their expression domains extend through the opisthosoma to the posterior growth zone. The overlap in expression domains of the posterior Hox genes is correlated with the absence of opisthosomal organs posterior to the tubular tracheae, which occur on the second opisthosomal segment. Together with the staggered profile of posterior Hox genes in spiders, these data suggest the involvement of abdominal-A and Abdominal-B in the evolution of heteronomous patterning of the chelicerate opisthosoma, providing a mechanism that helps explain the morphological diversity of chelicerates.
    Evolution & Development 09/2012; 14(5):450-63. DOI:10.1111/j.1525-142X.2012.00565.x · 2.72 Impact Factor
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