Rotiferan Hox Genes Give New Insights into the Evolution of Metazoan Bodyplans

Overview

Journal Nat Commun

Specialty Biology

Date 2017 Apr 6

PMID 28377584

Citations 21

Authors

Andreas C Frobius

Peter Funch

Affiliations

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Abstract

The phylum Rotifera consists of minuscule, nonsegmented animals with a unique body plan and an unresolved phylogenetic position. The presence of pharyngeal articulated jaws supports an inclusion in Gnathifera nested in the Spiralia. Comparison of Hox genes, involved in animal body plan patterning, can be used to infer phylogenetic relationships. Here, we report the expression of five Hox genes during embryogenesis of the rotifer Brachionus manjavacas and show how these genes define different functional components of the nervous system and not the usual bilaterian staggered expression along the anteroposterior axis. Sequence analysis revealed that the lox5-parapeptide, a key signature in lophotrochozoan and platyhelminthean Hox6/lox5 genes, is absent and replaced by different signatures in Rotifera and Chaetognatha, and that the MedPost gene, until now unique to Chaetognatha, is also present in rotifers. Collectively, our results support an inclusion of chaetognaths in gnathiferans and Gnathifera as sister group to the remaining spiralians.Rotifers are microscopic animals with an unusual, nonsegmented body plan consisting of a head, trunk and foot. Here, Fröbius and Funch investigate the role of Hox genes-which are widely used in animal body plan patterning-in rotifer embryogenesis and find non-canonical expression in the nervous system.

Citing Articles

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A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they "animal seeds"?.

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References

Sorensen M . Further structures in the jaw apparatus of Limnognathia maerski (Micrognathozoa), with notes on the phylogeny of the Gnathifera. J Morphol. 2002; 255(2):131-45. DOI: 10.1002/jmor.10038. View

Burke A, Nelson C, Morgan B, Tabin C . Hox genes and the evolution of vertebrate axial morphology. Development. 1995; 121(2):333-46. DOI: 10.1242/dev.121.2.333. View

Cavalier-Smith T . A revised six-kingdom system of life. Biol Rev Camb Philos Soc. 1998; 73(3):203-66. DOI: 10.1017/s0006323198005167. View

Shimotori T, Goto T . Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes. Dev Growth Differ. 2001; 43(4):371-82. DOI: 10.1046/j.1440-169x.2001.00583.x. View

Ferrier D, Minguillon C, Holland P, Garcia-Fernandez J . The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol Dev. 2001; 2(5):284-93. DOI: 10.1046/j.1525-142x.2000.00070.x. View

Dunn C, Hejnol A, Matus D, Pang K, Browne W, Smith S . Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 2008; 452(7188):745-9. DOI: 10.1038/nature06614. View

Telford M . Turning Hox "signatures" into synapomorphies. Evol Dev. 2001; 2(6):360-4. DOI: 10.1046/j.1525-142x.2000.00075.x. View

Struck T, Wey-Fabrizius A, Golombek A, Hering L, Weigert A, Bleidorn C . Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. Mol Biol Evol. 2014; 31(7):1833-49. DOI: 10.1093/molbev/msu143. View

Philippe H, Brinkmann H, Copley R, Moroz L, Nakano H, Poustka A . Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature. 2011; 470(7333):255-8. PMC: 4025995. DOI: 10.1038/nature09676. View

10.

Pierce R, Wu W, Hirai H, Ivens A, Murphy L, Noel C . Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni. Mol Biol Evol. 2005; 22(12):2491-503. DOI: 10.1093/molbev/msi239. View

11.

Matus D, Halanych K, Martindale M . The Hox gene complement of a pelagic chaetognath, Flaccisagitta enflata. Integr Comp Biol. 2011; 47(6):854-64. DOI: 10.1093/icb/icm077. View

12.

Matus D, Copley R, Dunn C, Hejnol A, Eccleston H, Halanych K . Broad taxon and gene sampling indicate that chaetognaths are protostomes. Curr Biol. 2006; 16(15):R575-6. DOI: 10.1016/j.cub.2006.07.017. View

13.

Averof M, Akam M . Hox genes and the diversification of insect and crustacean body plans. Nature. 1995; 376(6539):420-3. DOI: 10.1038/376420a0. View

14.

Ronquist F, Huelsenbeck J . MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12):1572-4. DOI: 10.1093/bioinformatics/btg180. View

15.

Laumer C, Bekkouche N, Kerbl A, Goetz F, Neves R, Sorensen M . Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol. 2015; 25(15):2000-6. DOI: 10.1016/j.cub.2015.06.068. View

16.

von Allmen G, Hogga I, Spierer A, Karch F, Bender W, Gyurkovics H . Splits in fruitfly Hox gene complexes. Nature. 1996; 380(6570):116. DOI: 10.1038/380116a0. View

17.

CARROLL S . Homeotic genes and the evolution of arthropods and chordates. Nature. 1995; 376(6540):479-85. DOI: 10.1038/376479a0. View

18.

Extavour C . Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol. 2011; 47(5):770-85. DOI: 10.1093/icb/icm027. View

19.

Lee P, Callaerts P, De Couet H, Martindale M . Cephalopod Hox genes and the origin of morphological novelties. Nature. 2003; 424(6952):1061-5. DOI: 10.1038/nature01872. View

20.

Balavoine G, de Rosa R, Adoutte A . Hox clusters and bilaterian phylogeny. Mol Phylogenet Evol. 2002; 24(3):366-73. DOI: 10.1016/s1055-7903(02)00237-3. View