No 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.
The gene decapentaplegic (dpp) and its homologs are essential for establishing the dorsoventral body axis in arthropods and vertebrates. However, the expression of dpp is not uniform among different arthropod groups. While this gene is expressed along the dorsal body region in insects, its expression occurs in a mesenchymal group of cells called cumulus in the early spider embryo. A cumulus-like structure has also been reported from centipedes, suggesting that it might be either an ancestral feature of arthropods or a derived feature (=synapomorphy) uniting the chelicerates and myriapods. To decide between these two alternatives, we analysed the expression patterns of a dpp ortholog in a representative of one of the closest arthropod relatives, the onychophoran Euperipatoides rowelli. Our data revealed unique expression patterns in the early mesoderm anlagen of the antennal segment and in the dorsal and ventral extra-embryonic tissue, suggesting a divergent role of dpp in these tissues in Onychophora. In contrast, the expression of dpp in the dorsal limb portions resembles that in arthropods, except that it occurs in the mesoderm rather than in the ectoderm of the onychophoran limbs. A careful inspection of embryos of E. rowelli revealed no cumulus-like accumulation of dpp expressing cells at any developmental stage, suggesting that this feature is either a derived feature of chelicerates or a synapomorphy uniting the chelicerates and myriapods.
Despite the different developmental modes in these onychophoran species, our data suggest that patterns of apoptosis are conserved among onychophorans. While apoptosis in the dorsal extra-embryonic tissue might contribute to dorsal closure-a process also known from arthropods-the involvement of apoptosis in ventral closure might be unique to onychophorans. Apoptosis in the placental stalk of P. hitoyensis is most likely a derived feature of the placentotrophic onychophorans. Developmental Dynamics 246:403-416, 2017. © 2017 Wiley Periodicals, Inc.
No abstract
Background NK genes are a group of homeobox transcription factors that are involved in various molecular pathways across bilaterians. They are typically divided into two subgroups, the NK cluster (NKC) and NK-linked genes (NKL). While the NKC genes have been studied in various bilaterians, corresponding data of many NKL genes are missing to date. To further investigate the ancestral roles of NK family genes, we analyzed the expression patterns of NKL genes in the onychophoran Euperipatoides rowelli . Results The NKL gene complement of E. rowelli comprises eight genes, including BarH , Bari , Emx , Hhex , Nedx , NK2.1 , vax and NK2.2 , of which only NK2.2 was studied previously. Our data for the remaining seven NKL genes revealed expression in different structures associated with the developing nervous system in embryos of E. rowelli . While NK2.1 and vax are expressed in distinct medial regions of the developing protocerebrum early in development, BarH , Bari , Emx , Hhex and Nedx are expressed in late developmental stages, after all major structures of the nervous system have been established. Furthermore, BarH and Nedx are expressed in distinct mesodermal domains in the developing limbs. Conclusions Comparison of our expression data to those of other bilaterians revealed similar patterns of NK2.1 , vax , BarH and Emx in various aspects of neural development, such as the formation of anterior neurosecretory cells mediated by a conserved molecular mechanism including NK2.1 and vax , and the development of the central and peripheral nervous system involving BarH and Emx . A conserved role in neural development has also been reported from NK2.2 , suggesting that the NKL genes might have been primarily involved in neural development in the last common ancestor of bilaterians or at least nephrozoans (all bilaterians excluding xenacoelomorphs). The lack of comparative data for many of the remaining NKL genes, including Bari , Hhex and Nedx currently hampers further evolutionary conclusions. Hence, future studies should focus on the expression of these genes in other bi...
The so-called extra-embryonic tissues are important for embryonic development in many animals, although they are not considered to be part of the germ band or the embryo proper. They can serve a variety of functions, such as nutrient uptake and waste removal, protection of the embryo against mechanical stress, immune response and morphogenesis. In insects, a subgroup of arthropods, extra-embryonic tissues have been studied extensively and there is increasing evidence that they might contribute more to embryonic development than previously thought. In this review, we provide an assessment of the occurrence and possible functions of extra-embryonic tissues in the closest arthropod relatives, onychophorans (velvet worms) and tardigrades (water bears). While there is no evidence for their existence in tardigrades, these tissues show a remarkable diversity across the onychophoran subgroups. A comparison of extra-embryonic tissues of onychophorans to those of arthropods suggests shared functions in embryonic nutrition and morphogenesis. Apparent contribution to the final form of the embryo in onychophorans and at least some arthropods supports the hypothesis that extra-embryonic tissues are involved in organogenesis. In order to account for this role, the commonly used definition of these tissues as ‘extra-embryonic’ should be reconsidered. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.
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