Expression of NK cluster genes in the onychophoran Euperipatoides rowelli: implications for the evolution of NK family genes in nephrozoans

Abstract

BackgroundUnderstanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this “urbilaterian” is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran Euperipatoides rowelli.ResultsWe identified nine transcripts of NK cluster genes in E. rowelli, including single copies of NK1, NK3, NK4, NK5, Msx, Lbx and Tlx, and two copies of NK6. All of these genes except for NK6.1 and NK6.2 are expressed in different mesodermal organs and tissues in embryos of E. rowelli, including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of NK3, NK5, NK6, Lbx and Msx in the developing nervous system. The same holds true for the NKL gene NK2.2, which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, NK1, Msx and Lbx are additionally expressed in a segment polarity-like pattern early in development—a feature that has been otherwise reported only from annelids.ConclusionOur results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex “urbilaterian” with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.Electronic supplementary materialThe online version of this article (10.1186/s13227-018-0105-2) contains supplementary material, which is available to authorized users.

Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

“…Consistent with the variable roles of BMP signaling in neuroectoderm specification, mediolateral neural gene expression patterns in hemichordates (Lowe et al, 2006), many spiralians (Martin-Duran et al, 2018;Monjo & Romero, 2015) and ecdysozoans [e.g., the onychophoran Euperipatoides rowelli (Treffkorn et al, 2018) and nematode C. elegans (Johnson & Chamberlin, 2008 (Arendt, 2018;Arendt & Nubler-Jung, 1999;Arendt et al, 2008;Arendt, Tosches, et al, 2016;Denes et al, 2007;Holland et al, 2013), all examined markers (nkx2.1/nkx2.2, pax6 and msx) are expressed around the circumference of the embryo of the hemichordate enteropneust Saccoglossus (Green, Norris, Terasaki, & Lowe, 2013;Lowe et al, 2003Lowe et al, , 2006 Figure 1a). Secondly, their expression profile is highly variable among spiralians (Figure 1a, see the Spiralia clade).…”

“…However, evo‐devo studies on other classes of bilaterians, especially those with paired nerve cords, suggest convergence of Nervous System Centralization, i.e., the absence of a condensed, mediolaterally patterned ventral nerve cord in the urbilaterian, or even urnephrozoan. Instead, it is proposed that CNS evolved independently in chordata, arthropodas and some annelids (Hejnol & Lowe, ; Martin‐Duran et al., ; Treffkorn et al., ).…”

“…At last, the dorsoventral markers are expressed with little association with the trunk neuroanatomies in the rotifer Epiphanes senta , a member of the sister lineage to all remaining Spiralia (Martin‐Duran et al., ). Dramatic variation also exists among ecdysozoans (Figure a, see the Ecdysozoa clade), i.e., on the contrary to the high conservation in arthropods (Arendt & Nubler‐Jung, ), the mediolateral gene expression pattern is absent in the onychophoran Euperipatoides rowelli (Treffkorn et al., ) and mostly disappears in the nematode C. elegans (Johnson & Chamberlin, ; Okkema et al., ; Palmer et al., ). But in both Drosophila and C. elegans , the orthologs of NPB specifier Msx are expressed in their lateral neural borders (Figure a, see the Ecdysozoa clade) and specify the cell fate of lateral CNS precursors and PNS precursors (Li et al., ).…”

“…Instead, it is proposed that CNS evolved independently in chordata, arthropodas and some annelids (Hejnol & Lowe, 2015;Martin-Duran et al, 2018;Treffkorn et al, 2018).…”

Analysis of Pigment-Dispersing Factor Neuropeptides and Their Receptor in a Velvet Worm

“…The whole coding sequence (CDS) of the identified Er-pdfr gene was amplified from previously synthesized cDNA of E. rowelli [see (82)] using gene-specific primers (Er_pdfr_HindIII_F:…”