Hox genes are the key regulators of axial regionalization of bilaterian animals. However, their main function is fulfilled differently in the development of animals from different evolutionary branches. Early patterning of the developing embryos by Hox gene expression in the representatives of protostomes (arthropods, mollusks) starts in the ectodermal cells. On the contrary, the instructive role of the mesoderm in the axial patterning was demonstrated for vertebrates. This makes it difficult to understand if during the axial regionalization of ancestral bilaterians Hox genes first expressed in the developing mesoderm or the ectoderm. To resolve this question, it is necessary to expand the number of models for investigation of the early axial patterning. Here, we show that three Hox genes of the polychaete Alitta virens (formerly Nereis virens, Annelida, Lophotrochozoa)—Hox2, Hox4, and Lox5—are expressed in the mesodermal anlagen of the three future larval chaetigerous segments in spatially colinear manner before the initiation of Hox expression in the larval ectoderm. This is the first evidence of sequential Hox gene expression in the mesoderm of protostomes to date.
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Akam M (1995) Hox genes and the evolution of diverse body plans. Philos Trans R Soc Lond Ser B Biol Sci 349(1329):313–319 Review
Andreeva TF, Cook C, Korchagina NM, Akam M, Dondya AK (2001) Cloning and analysis of structural organization of Hox genes in the polychaete Nereis virens. Ontogenez 32:225–233 [Article in Russian]
Barak H, Preger-Ben Noon E, Reshef R (2012) Comparative spatiotemporal analysis of Hox gene expression in early stages of intermediate mesoderm formation. Dev Dyn 241(10):1637–1649
Bardine N, Lamers G, Wacker S, Donow C, Knoechel W, Durston A (2014) Vertical signalling involves transmission of Hox information from gastrula mesoderm to neuroectoderm. PLoS One 9(12):e115208. doi:10.1371/journal.pone.0115208
Biscotti MA, Canapa A, Forconi M, Barucca M (2014) Hox and ParaHox genes: a review on molluscs. Genesis 52(12):935–945
David B, Mooi R (2014) How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo 5:22
Duboule D (1994) Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl:135–142
Durston AJ, Zhu K (2015) A time space translation hypothesis for vertebrate axial patterning. Semin Cell Dev Biol 42:86–93. doi:10.1016/j.semcdb.2015.06.001
Fischer AH, Henrich T, Arendt D (2010) The normal development of Platynereis dumerilii (Nereididae, Annelida. Front Zool 7:31. doi:10.1186/1742-9994-7-31
Forlani S, Lawson KA, Deschamps J (2003) Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 130:3807–3819
Fröbius AC, Matus DQ, Seaver EC (2008) Genomic organization and expression demonstrate spatial and temporal Hox gene colinearity in the lophotrochozoan Capitella sp. I. PLoS One 3(12):e4004. doi:10.1371/journal.pone.0004004
Holland PW (2013) Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol 2(1):31–45
Holland PW, Garcia-Fernàndez J (1996) Hox genes and chordate evolution. Dev Biol 173(2):382–395
Hughes CL, Kaufman TC (2002) Hox genes and the evolution of the arthropod body plan. Evol Dev 4(6):459–499
Iimura T, Pourquie O (2006) Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442:568–571
Irvine SQ, Martindale MQ (2000) Expression patterns of anterior hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev Biol 217(2):333–351
Janssen R, Eriksson BJ, Tait NN, Budd GE (2014) Onychophoran Hox genes and the evolution of arthropod Hox gene expression. Front Zool 11(1):22. doi:10.1186/1742-9994-11-22
Kourakis MJ, Master VA, Lokhorst DK, Nardelli-Haefliger D, Wedeen CJ, Martindale MQ, Shankland M (1997) Conserved anterior boundaries of Hox gene expression in the central nervous system of the leech Helobdella. Dev Biol 190(2):284–300
Kulakova M, Bakalenko N, Novikova E, Cook CE, Eliseeva E, Steinmetz PR, Kostyuchenko RP, Dondua A, Arendt D, Akam M, Andreeva T (2007) Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa. Dev Genes Evol 217(1):39–54
Lacalli T (2014) Echinoderm conundrums: Hox genes, heterochrony, and an excess of mouths. EvoDevo 5(1):46. doi:10.1186/2041-9139-5-46
Marlow H, Tosches MA, Tomer R, Steinmetz PR, Lauri A, Larsson T, Arendt D (2014) Larval body patterning and apical organs are conserved in animal evolution. BMC Biol 12. doi:10.1186/1741-7007-12-7
Peterson KJ, Davidson EH (2000) Regulatory evolution and the origin of the bilaterians. Proc Natl Acad Sci U S A 97(9):4430–4433 Review
Wacker SA, Jansen HJ, McNulty CL, Houtzager E, Durston AJ (2004) Timed interactions between the Hox expressing non-organiser mesoderm and the Spemann organiser generate positional information during vertebrate gastrulation. Dev Biol 268:207–219
Weigert A, Helm C, Meyer M, Nickel B, Arendt D, Hausdorf B, Santos SR, Halanych KM, Purschke G, Bleidorn C, Struck TH (2014) Illuminating the base of the annelid tree using transcriptomics. Mol Biol Evol 31(6):1391–1401
Wilson EB (1892) The cell-lineage of Nereis. A contribution to the cytogeny of the annelid body. J Morphol 7(3):361–480
The authors thank Olga B. Lavrova for maintaining the A. virens culture in the laboratory of experimental embryology and Alexander Y. Nesterenko for participating in the material collection. We are also grateful to the staff of the White Sea Biological Station “Kartesh” (Zoological Institute, Russian Academy of Science) for providing an opportunity to collect A. virens. We thank the “Chromas” center for the opportunity to use the workstation Leica DMRXA. The research was supported by RFBR grants 14-04-31683-mol-a and 14-04-01531-a and the grant from St. Petersburg State University № 22.214.171.1244.
Milana A. Kulakova performed WMISH and analyzed the results. Elena L. Novikova drafted the manuscript. All the authors participated in the maintenance of the larval culture and material preparation. All the authors have analyzed and discussed the results, read, and approved the final manuscript.
The authors declare that they have no competing interests.
Communicated by David A. Weisblat
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Kulakova, M.A., Bakalenko, N.I. & Novikova, E.L. Early mesodermal expression of Hox genes in the polychaete Alitta virens (Annelida, Lophotrochozoa). Dev Genes Evol 227, 69–74 (2017). https://doi.org/10.1007/s00427-016-0563-2
- Hox genes