Expression of Six3 and Otx in Solenogastres (Mollusca) Supports an Ancestral Role in Bilaterian Anterior-posterior Axis Patterning

Overview

Journal Evol Dev

Specialty Biology

Date 2017 Dec 16

PMID 29243871

Citations 4

Authors

Emanuel Redl

Maik Scherholz

Tim Wollesen

Christiane Todt

Andreas Wanninger

Affiliations

Soon will be listed here.

Abstract

The homeodomain transcription factors six3 and otx are involved in patterning the anterior body and parts of the central nervous system (CNS) in bilaterians. Their similar expression patterns have been used as an argument for homology of heads, brains, segmentation, and ciliated larvae. We investigated the developmental expression of six3 and otx in the aplacophoran mollusk Wirenia argentea. Six3 is expressed in subepithelial cells delimiting the apical organ of the solenogaster pericalymma larva. Otx is expressed in cells of the prototroch and adjacent regions as well as in posterior extensions of the prototrochal expression domain. Advanced larvae also show pretrochal otx expression in the developing CNS. Comparative analysis of six3 and otx expression in bilaterians argues for an ancestral function in anterior-posterior body axis patterning but, due to its presence in animals lacking a head and/or a brain, not necessarily for the presence of these morphological structures in the last common ancestor (LCA) of bilaterians. Likewise, the hypothesis that the posterior border of otx expression corresponds to the border between the unsegmented head and the segmented trunk of the LCA of protostomes is not supported, since otx is extensively expressed in the trunk in W. argentea and numerous other protostomes.

Citing Articles

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Wanninger A, Wollesen T Biol Rev Camb Philos Soc. 2018; 94(1):102-115.

PMID: 29931833 PMC: 6378612. DOI: 10.1111/brv.12439.

Expression of six3 and otx in Solenogastres (Mollusca) supports an ancestral role in bilaterian anterior-posterior axis patterning.

Redl E, Scherholz M, Wollesen T, Todt C, Wanninger A Evol Dev. 2017; 20(1):17-28.

PMID: 29243871 PMC: 5814893. DOI: 10.1111/ede.12245.

References

Sinigaglia C, Busengdal H, Leclere L, Technau U, Rentzsch F . The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol. 2013; 11(2):e1001488. PMC: 3586664. DOI: 10.1371/journal.pbio.1001488. View

Boyle M, Yamaguchi E, Seaver E . Molecular conservation of metazoan gut formation: evidence from expression of endomesoderm genes in Capitella teleta (Annelida). Evodevo. 2015; 5:39. PMC: 4407770. DOI: 10.1186/2041-9139-5-39. View

Arendt D, Technau U, Wittbrodt J . Evolution of the bilaterian larval foregut. Nature. 2001; 409(6816):81-5. DOI: 10.1038/35051075. View

Hiebert L, Maslakova S . Hox genes pattern the anterior-posterior axis of the juvenile but not the larva in a maximally indirect developing invertebrate, Micrura alaskensis (Nemertea). BMC Biol. 2015; 13:23. PMC: 4426647. DOI: 10.1186/s12915-015-0133-5. View

Lowe C, Wu M, Salic A, Evans L, Lander E, Stange-Thomann N . Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell. 2003; 113(7):853-65. DOI: 10.1016/s0092-8674(03)00469-0. View

Boyle J, Lew A . An inexpensive alternative to glassmilk for DNA purification. Trends Genet. 1995; 11(1):8. DOI: 10.1016/s0168-9525(00)88977-5. View

Ogura A, Yoshida M, Moritaki T, Okuda Y, Sese J, Shimizu K . Loss of the six3/6 controlling pathways might have resulted in pinhole-eye evolution in Nautilus. Sci Rep. 2013; 3:1432. PMC: 3594755. DOI: 10.1038/srep01432. View

Marlow H, Tosches M, Tomer R, Steinmetz P, Lauri A, Larsson T . Larval body patterning and apical organs are conserved in animal evolution. BMC Biol. 2014; 12:7. PMC: 3939940. DOI: 10.1186/1741-7007-12-7. View

Li Y, Brown S, Hausdorf B, Tautz D, Denell R, Finkelstein R . Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum. Dev Genes Evol. 2013; 206(1):35-45. DOI: 10.1007/s004270050028. View

10.

Hinman V, Nguyen A, Davidson E . Expression and function of a starfish Otx ortholog, AmOtx: a conserved role for Otx proteins in endoderm development that predates divergence of the eleutherozoa. Mech Dev. 2003; 120(10):1165-76. DOI: 10.1016/j.mod.2003.08.002. View

11.

Poustka A, Kuhn A, Groth D, Weise V, Yaguchi S, Burke R . A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol. 2007; 8(5):R85. PMC: 1929154. DOI: 10.1186/gb-2007-8-5-r85. View

12.

Hiebert L, Maslakova S . Expression of Hox, Cdx, and Six3/6 genes in the hoplonemertean Pantinonemertes californiensis offers insight into the evolution of maximally indirect development in the phylum Nemertea. Evodevo. 2015; 6:26. PMC: 4524027. DOI: 10.1186/s13227-015-0021-7. View

13.

Shoguchi E, Harada Y, Numakunai T, Satoh N . Expression of the otx gene in the ciliary bands during sea cucumber embryogenesis. Genesis. 2000; 27(2):58-63. DOI: 10.1002/1526-968x(200006)27:2<58::aid-gene20>3.0.co;2-8. View

14.

Dunn E, Moy V, Angerer L, Angerer R, Morris R, Peterson K . Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian. Evol Dev. 2007; 9(1):10-24. DOI: 10.1111/j.1525-142X.2006.00134.x. View

15.

Perry K, Lyons D, Truchado-Garcia M, Fischer A, Helfrich L, Johansson K . Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc Crepidula. Dev Dyn. 2015; 244(10):1215-48. DOI: 10.1002/dvdy.24308. View

16.

Simeone A, Acampora D, Mallamaci A, Stornaiuolo A, DApice M, Nigro V . A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 1993; 12(7):2735-47. PMC: 413524. DOI: 10.1002/j.1460-2075.1993.tb05935.x. View

17.

Vellutini B, Martin-Duran J, Hejnol A . Cleavage modification did not alter blastomere fates during bryozoan evolution. BMC Biol. 2017; 15(1):33. PMC: 5408385. DOI: 10.1186/s12915-017-0371-9. View

18.

Posnien N, Koniszewski N, Hein H, Bucher G . Candidate gene screen in the red flour beetle Tribolium reveals six3 as ancient regulator of anterior median head and central complex development. PLoS Genet. 2012; 7(12):e1002416. PMC: 3245309. DOI: 10.1371/journal.pgen.1002416. View

19.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

20.

Janssen R, Budd G, Damen W . Gene expression suggests conserved mechanisms patterning the heads of insects and myriapods. Dev Biol. 2011; 357(1):64-72. DOI: 10.1016/j.ydbio.2011.05.670. View