Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis

• DOI: 10.1016/j.ydbio.2008.02.013
• Publication Date: 2008-02-22T16:25:11Z
• Authors: Alexandra Saudemont; Nicolas Dray; Bruno Hudry; Martine Le Gouar; Michel Vervoort; Guillaume Balavoine
• Keywords: MESH: Sequence Analysis, DNA; MESH: DNA, Complementary/genetics; Posterior growth; DNA, Complementary; MESH: Homeodomain Proteins/metabolism*; Annelida; Molecular Sequence Data; MESH: Muscle Development/physiology*; MESH: Somites/embryology*; MESH: Base Sequence; Bilaterian evolution; Muscle Development; MESH: DNA Primers/genetics; 03 medical and health sciences; MESH: In Situ Hybridization; Segmentation; Animals; Cluster Analysis; MESH: Animals; MESH: Gene Expression Regulation, Developmental*; MESH: Annelida/embryology*; MESH: Phylogeny; MESH: Heart/embryology*; [SDV.BDD]Life Sciences [q-bio]/Development Biology; Molecular Biology; Platynereis; In Situ Hybridization; Phylogeny; DNA Primers; Homeodomain Proteins; 0303 health sciences; MESH: Molecular Sequence Data; Annelid; NK homeobox genes; Base Sequence; MESH: Somites/metabolism; [SDV.BA]Life Sciences [q-bio]/Animal biology; Gene Expression Regulation, Developmental; Heart; Cell Biology; Sequence Analysis, DNA; MESH: Cluster Analysis; tinman; NK homeobox genes tinman; Somites; MESH: Homeodomain Proteins/genetics; Developmental Biology

NK genes are related pan-metazoan homeobox genes. In the fruitfly, NK genes are clustered and involved in patterning various mesodermal derivatives during embryogenesis. It was therefore suggested that the NK cluster emerged in evolution as an ancestral mesodermal patterning cluster. To test this hypothesis, we cloned and analysed the expression patterns of the homologues of NK cluster genes Msx, NK4, NK3, Lbx, Tlx, NK1 and NK5 in the marine annelid Platynereis dumerilii, a representative of trochozoans, the third great branch of bilaterian animals alongside deuterostomes and ecdysozoans. We found that most of these genes are involved, as they are in the fly, in the specification of distinct mesodermal derivatives, notably subsets of muscle precursors. The expression of the homologue of NK4/tinman in the pulsatile dorsal vessel of Platynereis strongly supports the hypothesis that the vertebrate heart derived from a dorsal vessel relocated to a ventral position by D/V axis inversion in a chordate ancestor. Additionally and more surprisingly, NK4, Lbx, Msx, Tlx and NK1 orthologues are expressed in complementary sets of stripes in the ectoderm and/or mesoderm of forming segments, suggesting an involvement in the segment formation process. A potentially ancient role of the NK cluster genes in segment formation, unsuspected from vertebrate and fruitfly studies so far, now deserves to be investigated in other bilaterian species, especially non-insect arthropods and onychophorans.