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Comparative Study
. 1998 Mar 17;95(6):3030-5.
doi: 10.1073/pnas.95.6.3030.

Homeobox genes in the ribbonworm Lineus sanguineus: evolutionary implications

M Kmita-Cunisse  1 , F Loosli, J Bièrne, W J Gehring
Affiliations
Comparative Study

Homeobox genes in the ribbonworm Lineus sanguineus: evolutionary implications

M Kmita-Cunisse et al. Proc Natl Acad Sci U S A. .

Abstract

From our current understanding of the genetic basis of development and pattern formation in Drosophila and vertebrates it is commonly thought that clusters of Hox genes sculpt the morphology of animals in specific body regions. Based on Hox gene conservation throughout the animal kingdom it is proposed that these genes and their role in pattern formation evolved early during the evolution of metazoans. Knowledge of the history of Hox genes will lead to a better understanding of the role of Hox genes in the evolution of animal body plans. To infer Hox gene evolution, reliable data on lower chordates and invertebrates are crucial. Among the lower triploblasts, the body plan of the ribbonworm Lineus (nemertini) appears to be close to the common ancestral condition of protostomes and deuterostomes. In this paper we present the isolation and identification of Hox genes in Lineus sanguineus. We find that the Lineus genome contains a single cluster of at least six Hox genes: two anterior-class genes, three middle-class genes, and one posterior-class gene. Each of the genes can be definitely assigned to an ortholog group on the basis of its homeobox and its flanking sequences. The most closely related homeodomain sequences are invariably found among the mouse or Amphioxus orthologs, rather than Drosophila and other invertebrates. This suggests that the ribbonworms have diverged relatively little from the last common ancestors of protostomes and deuterostomes, the urbilateria.

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Figures

Figure 1
Figure 1
Scheme of Lineus body organization. The different body regions (R) along the A-P axis are numbered starting from the anterior end and are characterized by the following structures: R1, cephalic glands, rhynchodeum, and eyes; R2, cerebral ganglia; R3, sensory cerebral organs; R4, postcerebral, preesophageal connective tissue; R5, mouth; R6, posterior esophagus and nephridia; R7, anterior intestine (gonads absent); R8, middle and posterior intestine plus gonads; R9, anus; R10, caudal end.
Figure 2
Figure 2
Evolutionary distance tree. Based on the neighbor-joining method including the complete 18S ribosomal RNA sequences of 33 species belonging to 16 different phyla, with special emphasis on platyhelminths. The nemertean listed is Prostoma eilhardi. The numbers at the nodes are percentages of 1,000 boot trap replicates that support the branch, with only values over 50% being represented. All branch lengths are drawn to scale. The choanoflagellate Sphaeroeca volvox is used as outgroup. The Fitch–Margoliash method gives the same topology. (Reproduced with permission from ref. .)
Figure 3
Figure 3
Sequence alignments of homeodomains and flanking sequences encoded by LsHox genes (Upper) plus caudal/Cdx and NK-1 orthologs (Lower). Dashes indicate amino acid identity between domains encoded by L. sanguineus homeobox genes and the most similar sequences from other phyla. Percentages indicated correspond to sequence identities within the homeodomain between L. sanguineus genes and the sequences from other phyla. The sequence comparison is limited to the small number of homeodomains known in protostomes for which complete sequence data are available.
Figure 4
Figure 4
Sequence alignments of the C-terminal domains encoded by the LsHox1 and LsHox7 genes with chordate OG-1 genes (Upper) and vertebrate PG-7 genes (Lower), respectively. Dashes indicate identical amino acids. Conservative changes and identical residues are boxed in.
Figure 5
Figure 5
Southern blot analysis of pulse-field gel. (A) Hybridization pattern obtained with the probe H3 (LsHox3 subclone). (B) Hybridization pattern obtained with the probe H7 (LsHox7 subclone). 1, uncut genomic DNA; 2, DNA digested with NotI; 3, DNA digested with PstI; 4, DNA partially digested with SacII. The same blot was hybridized successively with both probes. The blot was first hybridized with the probe H3. The autoradiogram was obtained after 12 hr of exposure. The blot was then dehybridized and hybridized again with the probe H7. The autoradiogram was obtained after 30 hr of exposure. The second hybridization has given signals of lower intensity and a higher background compared with the first hybridization. Both probes give the same hybridization pattern except in the case of DNA digested with PstI. This enzyme was used as a control because we expected, in this case, a different hybridization pattern with the two probes. The results confirm first, that no signal was left after dehybridization and second, that the hybridization patterns obtained for each probe are specific.
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