A hemocyanin from the Onychophora and the emergence of respiratory proteins

Kusche, Kristina; Ruhberg, Hilke; Burmester, Thorsten

doi:10.1073/pnas.152241199

Cited by 91 publications

(44 citation statements)

References 38 publications

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“…Together with molecular datasets (e.g. Boore et al 1998;Shultz & Regier 2000;Giribet et al 2001;Kusche et al 2002;Pisani et al 2004;Petrov & Vladychenskaya 2005;Regier et al 2005;Mallatt & Giribet 2006), these studies contributed considerably to the new discussion on arthropod relationships (e.g. Whitington & Bacon 1997;Dohle 2001;Richter 2002;Whitington 2004;Giribet et al 2005).…”

Section: Introductionmentioning

confidence: 99%

Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata

Ungerer

Scholtz

2007

Proc. R. Soc. B.

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The complex spatio-temporal patterns of development and anatomy of nervous systems play a key role in our understanding of arthropod evolution. However, the degree of resolution of neural processes is not always detailed enough to claim homology between arthropod groups. One example is neural precursors and their progeny in crustaceans and insects. Pioneer neurons of crustaceans and insects show some similarities that indicate homology. In contrast, the differentiation of insect and crustacean neuroblasts (NBs) shows profound differences and their homology is controversial. For Drosophila and grasshoppers, the complete lineage of several NBs up to formation of pioneer neurons is known. Apart from data on median NBs no comparable results exist for Crustacea. Accordingly, it is not clear where the crustacean pioneer neurons come from and whether there are NBs lateral to the midline homologous to those of insects. To fill this gap, individual NBs in the ventral neuroectoderm of the crustacean Orchestia cavimana were labelled in vivo with a fluorescent dye. A partial neuroblast map was established and for the first time lineages from individual NBs to identified pioneer neurons were established in a crustacean. Our data strongly suggest homology of NBs and their lineages, providing further evidence for a close insect-crustacean relationship.Keywords: Drosophila; evolution; arthropods; neurogenesis; cell lineage INTRODUCTIONDespite the overall similarities of the central nervous system (CNS) between the major arthropod groups, its early development shows some distinct differences at the cellular level. In myriapods and chelicerates, clusters of neural precursors immigrate from the ventral neuroectoderm and differentiate directly into neurons or glia cells to form the ventral CNS (figure 1; Stollewerk et al. 2001;Mittmann 2002;Stollewerk & Chipman 2006). In contrast, insects and crustaceans form their ventral CNS via neuroblasts (NBs), large neural precursor cells dividing in an asymmetrical stem cell mode to produce columns of ganglion mother cells (GMCs). At least in insects, each GMC in turn divides once to generate ganglion cells (GCs) that differentiate into neurons and/or glia cells (figure 1; insects: Wheeler 1891, Bate 1976, Doe & Goodman 1985, Hartenstein et al. 1987, Truman & Ball 1998 crustaceans: McMurrich 1895, Dohle 1976, Scholtz 1992, Gerberding 1997, Harzsch 2001.In 1984, Thomas et al. (1984) detected a set of early differentiating neurons, responsible for pioneering major axon pathways in the embryonic CNS of insects and crustaceans, which led them to propose a common plan for neurogenesis in arthropods. A series of subsequent studies at the level of individually identified neurons including position, axon morphology and timing of outgrowth confirmed the existence of a set of homologous pioneer neurons in insects and crustaceans that finds no counterpart in myriapods (Whitington et al.

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Section: Introductionmentioning

confidence: 99%

Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata

Ungerer

Scholtz

2007

Proc. R. Soc. B.

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“…Although the phylogenetic position of onychophorans is still debated, many phylogenies group them with euarthropods and possibly tardigrades in the phylum Arthropoda; thus onychophorans share a common ancestor with euarthropods (8,(19)(20)(21)(22)(23). Analyses of neurogenesis in onychophorans suggests that, similar to insects and crustaceans, single neural precursors are formed in the neuroectoderm, rather than groups of cells as seen in chelicerates and myriapods (24)(25)(26).…”

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confidence: 99%

Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis

Eriksson

Stollewerk

2010

Proc. Natl. Acad. Sci. U.S.A.

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One of the controversial debates on euarthropod relationships centers on the question as to whether insects, crustaceans, and myriapods (Mandibulata) share a common ancestor or whether myriapods group with the chelicerates (Myriochelata). The debate was stimulated recently by studies in chelicerates and myriapods that show that neural precursor groups (NPGs) segregate from the neuroectoderm generating the nervous system, whereas in insects and crustaceans the nervous tissue is produced by stem cells. Do the shared neural characters of myriapods and chelicerates represent derived characters that support the Myriochelata grouping? Or do they rather reflect the ancestral pattern? Analyses of neurogenesis in a group closely related to euarthropods, the onychophorans, show that, similar to insects and crustaceans, single neural precursors are formed in the neuroectoderm, potentially supporting the Myriochelata hypothesis. Here we show that the nature and the selection of onychophoran neural precursors are distinct from euarthropods. The onychophoran nervous system is generated by the massive irregular segregation of single neural precursors, contrasting with the limited number and stereotyped arrangement of NPGs/stem cells in euarthropods. Furthermore, neural genes do not show the spatiotemporal pattern that sets up the precise position of neural precursors as in euarthropods. We conclude that neurogenesis in onychophorans largely does not reflect the ancestral pattern of euarthropod neurogenesis, but shows a mixture of derived characters and ancestral characters that have been modified in the euarthropod lineage. Based on these data and additional evidence, we suggest an evolutionary sequence of arthropod neurogenesis that is in line with the Mandibulata hypothesis.achaete-scute homologue | euarthropod phylogeny | Notch signaling

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“…Previous phylogenetic reconstructions between mollusc and arthropod type-3 copper genes have indicated that these proteins have evolved independently (Burmester and Scheller 1996, Decker and Terwilliger 2000, Burmester 2002, Kusche et al 2002. Here, I demonstrated that mollusc and arthropod type-3 copper genes belong to different subclasses (α-and β-subclass, respectively), supporting previous assertions of their independent origin and convergent evolution.…”

Section: Structural Comparison Of Type-3 Copper Protein Active Sites supporting

confidence: 85%

Investigation of gene family evolution and the molecular basis of shell formation in molluscs

Aguilera¹

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Since the emergence of shell-bearing molluscs in the Early Cambrian, diverse shell forms have evolved. Modern molluscs are renowned for a highly complex and robust shell, which is the product of the orchestrated expression of genes and secretion of a large number of proteins and other macromolecules from the epithelium of a specialised organ called the mantle. Molluscan shells display remarkable morphological diversity, structure and ornamentation, however the molecular mechanisms underlying the evolution and formation of the shell remain largely unknown. In this thesis, I seek to investigate the nature of the mantle transcriptome focussing on the timing of origin of genes expressed in the mantle and the evolutionary history of gene families that encode secreted proteins in representatives of bivalve and gastropod species.First, by comparative transcriptomics of the mantle, I determined the origin and evolution of gene families expressed in this organ. Gene origin analyses show that most genes expressed in the mantle are taxon-restricted innovations (i.e. unique to a particular species), although a large number of genes arose along the stems leading to the bilaterian and molluscan last common ancestors. Focussing on gene families that encode secreted proteins that are likely to be embedded within the shell and/or to regulate shell construction, I found that these are comprised of both ancient and lineage-specific gene families. The evolution of these gene families is highly dynamic with prolific gene family gains and losses over evolutionary time. By comparing sequences, I also detected indications of positively selected gene families over molluscan evolution. These gene families show unique patterns of enrichment of protein domains, and presumably molecular functions, that are taxa-specific, suggesting that bivalves and gastropods use almost completely different secretory repertoire to construct their shells.I then focused on an ancient gene family expressed in the molluscan mantles -the tyrosinase gene family -to understand how a conserved gene family has been co-opted into the biomineralisation pathway. I found no evidence of large-scale expansion of tyrosinase genes in gastropods, whereas tyrosinase genes in bivalves have undergone substantial independent gene expansions in at least two lineages (Pinctada spp. and Crassostrea gigas), and that the resulting gene duplicates have been co-opted into the mantle gene regulatory network. Many of the tyrosinase genes are found in clusters within the genomes and are expressed at relatively high levels in the mantle. Detailed 3 comparisons of tyrosinase gene expression in different regions of the mantle in two closely related pearl oysters, P. maxima and P. margaritifera, reveal that recently evolved orthologous genes have unique expression profiles across the mantle with high expression levels at the distal mantle edge, suggesting roles in colouration and/or prismatic shell layer construction. Differences in expression levels are consistent with the rapid evo...

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A hemocyanin from the Onychophora and the emergence of respiratory proteins

Cited by 91 publications

References 38 publications

Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata

Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata

Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis

Investigation of gene family evolution and the molecular basis of shell formation in molluscs

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