Matus DQ et al. (2006), Molecular evidence for deep evolutionary roots ...

XB-ART-137

Proc Natl Acad Sci U S A 2006 Jul 25;10330:11195-200. doi: 10.1073/pnas.0601257103.

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Molecular evidence for deep evolutionary roots of bilaterality in animal development.

Matus DQ , Pang K , Marlow H , Dunn CW , Thomsen GH , Martindale MQ .

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Nearly all metazoans show signs of bilaterality, yet it is believed the bilaterians arose from radially symmetric forms hundreds of millions of years ago. Cnidarians (corals, sea anemones, and "jellyfish") diverged from other animals before the radiation of the Bilateria. They are diploblastic and are often characterized as being radially symmetrical around their longitudinal (oral-aboral) axis. We have studied the deployment of orthologs of a number of family members of developmental regulatory genes that are expressed asymmetrically during bilaterian embryogenesis from the sea anemone, Nematostella vectensis. The secreted TGF-beta genes Nv-dpp, Nv-BMP5-8, six TGF-beta antagonists (NvChordin, NvNoggin1, NvNoggin2, NvGremlin, NvFollistatin, and NvFollistatin-like), the homeodomain proteins NvGoosecoid (NvGsc) and NvGbx, and the secreted guidance factor, NvNetrin, were studied. NvDpp, NvChordin, NvNoggin1, NvGsc, and NvNetrin are expressed asymmetrically along the axis perpendicular to the oral-aboral axis, the directive axis. Furthermore, NvGbx, and NvChordin are expressed in restricted domains on the left and right sides of the body, suggesting that the directive axis is homologous with the bilaterian dorsal-ventral axis. The asymmetric expression of NvNoggin1 and NvGsc appear to be maintained by the canonical Wnt signaling pathway. The asymmetric expression of NvNoggin1, NvNetrin, and Hox orthologs NvAnthox7, NvAnthox8, NvAnthox1a, and NvAnthox6, in conjunction with the observation that NvNoggin1 is able to induce a secondary axis in Xenopus embryos argues that N. vectensis could possess antecedents of the organization of the bilaterian central nervous system.

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Species referenced: Xenopus laevis
Genes referenced: bmp5 cer1 dspp fst grem1 gsc nbl1 nog

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	Fig. 12. Bayesian consensus tree showing orthology of N. vectensis NvGremlin to Cerberus/DAN/Gremlin metazoan genes. A Bayesian phylogenetic analysis was conducted by using the DAN domain of metazoan Cerberus, DAN, and gremlin metazoan orthologs, using the wag amino acid model option in MRBAYES with 1,000,000 generations sampled every 100 generations and four chains, with four independent runs. A consenus tree was produced with PAUP*4.0B10 from the last 9,500 trees of each run, representing 3,800,000 stationary generations. Numbers above branches represent posterior probabilities, calculated from this consensus. N. vectensis possesses one member of this gene family that shows a sister group relationship to the gremlin metazoan genes.
	Fig. 13. Bayesian consensus tree showing orthology of NvNetrin to other metazoan netrin genes. A Bayesian phylogenetic analysis was conducted by using near-full-length amino acid sequence of metazoan netrins, using the wag amino acid model option in MRBAYES with 1,000,000 generations sampled every 100 generations and four chains, with four independent runs. A consenus tree was produced with PAUP*4.0B10 from the last 9,500 trees of each run, representing 3,800,000 stationary generations. Numbers above branches represent posterior probabilities, calculated from this consensus. N. vectensis possesses one member of this gene family that shows a sister group relationship to the cephalochordate netrin gene, Amphinetrin, and appears to be more closely related to chordate netrin genes than protostome netrins.
	Fig. 14. Bayesian phylogenetic analysis of metazoan noggin genes. A Bayesian phylogenetic analysis was conducted by using near-full-length amino acid sequences of metazoan noggin orthologs, using the wag amino acid model option in MRBAYES with 1,000,000 generations sampled every 100 generations and four chains. A consenus tree was produced with PAUP*4.0B10 from the last 9,500 trees representing 950,000 stationary generations. Numbers above branches represent posterior probabilities, calculated from this consensus. The two N. vectensis noggin genes (NvNoggin1 and NvNoggin2) show definitive orthology to other metazoan, protostome, and deuterostome noggin orthologs. NvNoggin1 appears to be more closely related to the vertebrate noggin genes.
	Fig. 15. Bayesian consensus tree showing orthology of N. vectensis Follistatin genes. A Bayesian phylogenetic analysis was conducted by using near-full-length amino acid sequences of metazoan follistatin orthologs, using the wag amino acid model option in MRBAYES with 1,000,000 generations sampled every 100 generations and four chains, with four independent runs. A consenus tree was produced with PAUP*4.0B10 from the last 9,500 trees of each run, representing 3,800,000 stationary generations. Numbers above branches represent posterior probabilities, calculated from this consensus. The two N. vectensis follistatin genes (NvFollistatin and NvFollistatin-like) show definitive orthology to other metazoan, protostome, and deuterostome follistatin orthologs.
	Fig. 16. Bayesian consensus tree showing orthology of N. vectensis homeodomain genes. A Bayesian phylogenetic analysis of the 60-aa homeodomain plus alignable flanking regions was conducted by using the wag amino acid model option with 1,000,000 generations sampled every 100 generations and four chains, using MRBAYES . A consensus tree was produced with PAUP*4.0B10 from the last 9,500 trees representing 950,000 stationary generations. Numbers above branches represent posterior probabilities, calculated from this consensus. The Bayesian analysis recovers distinct homeodomain gene subclasses (Otx/Otd, Gsc, Gbx, Exd/Pbx, and Prd classes) and shows clear orthology for the N. vectensis homeodomain genes, NvOtxA, NvGsc, NvGbx, and NvExd, with metazoan representative genes of the same homeodomain subclass. Colors represent homeodomain gene subclasses, and arrows denote N. vectensis representative genes. Nexus alignment files and accession numbers are available on request.
	Fig. 17. Conserved dorsalizing activity of cnidarian and vertebrate Noggins. Xenopus embryos at the 16-cell stage were injected into one ventral, vegetal blastomere with synthetic mRNA encoding pGEM-7 vector (Control, 0.5 ng), Xenopus Noggin (XNoggin, 100 pg), or N. vectensis Noggin1 (NvNoggin1, 100 pg) as indicated. Arrows point to ectopic axes characteristic of Noggin-mediated BMP inhibition (1). Representative examples of ectopic axial structures are shown, and ectopic axes or otherwise dorsalized ventro-posterior tissues were generated in 0% of pGEM-7 (n =34), 67% of XNoggin (n = 17), and 74% of NvNoggin1 (n =27)-injected embryos.

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