Publications by authors named "Natascha Turetzek"

13 Publications

  • Page 1 of 1

Candidate gene screen for potential interaction partners and regulatory targets of the Hox gene labial in the spider Parasteatoda tepidariorum.

Dev Genes Evol 2020 03 8;230(2):105-120. Epub 2020 Feb 8.

Institut für Allgemeine Zoologie und Entwicklungsbiologie, AG Zoologie mit dem Schwerpunkt Molekulare Entwicklungsbiologie, Justus-Liebig-Universität Gießen, Heinrich-Buff-Ring 38, 35392, Gießen, Germany.

The Hox gene labial (lab) governs the formation of the tritocerebral head segment in insects and spiders. However, the morphology that results from lab action is very different in the two groups. In insects, the tritocerebral segment (intercalary segment) is reduced and lacks appendages, whereas in spiders the corresponding segment (pedipalpal segment) is a proper segment including a pair of appendages (pedipalps). It is likely that this difference between lab action in insects and spiders is mediated by regulatory targets or interacting partners of lab. However, only a few such genes are known in insects and none in spiders. We have conducted a candidate gene screen in the spider Parasteatoda tepidariorum using as candidates Drosophila melanogaster genes known to (potentially) interact with lab or to be expressed in the intercalary segment. We have studied 75 P. tepidariorum genes (including previously published and duplicated genes). Only 3 of these (proboscipedia-A (pb-A) and two paralogs of extradenticle (exd)) showed differential expression between leg and pedipalp. The low success rate points to a weakness of the candidate gene approach when it is applied to lineage specific organs. The spider pedipalp has no counterpart in insects, and therefore relying on insect data apparently cannot identify larger numbers of factors implicated in its specification and formation. We argue that in these cases a de novo approach to gene discovery might be superior to the candidate gene approach.
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http://dx.doi.org/10.1007/s00427-020-00656-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7128011PMC
March 2020

, a new and highly conserved key factor in arthropod dorsal-ventral (DV) limb patterning.

Evodevo 2019 8;10:28. Epub 2019 Nov 8.

1Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, Uppsala, Sweden.

Forkhead box (Fox) transcription factors evolved early in animal evolution and represent important components of conserved gene regulatory networks (GRNs) during animal development. Most of the researches concerning Fox genes, however, are on vertebrates and only a relatively low number of studies investigate Fox gene function in invertebrates. In addition to this shortcoming, the focus of attention is often restricted to a few well-characterized Fox genes such as (), () and . Although arthropods represent the largest and most diverse animal group, most other Fox genes have not been investigated in detail, not even in the arthropod model species . In a general gene expression pattern screen for panarthropod Fox genes including the red flour beetle , the pill millipede , the common house spider , and the velvet worm , we identified a Fox gene with a highly conserved expression pattern along the ventral ectoderm of arthropod and onychophoran limbs. Functional investigation of in reveals a hitherto unrecognized important function of FoxB upstream of () and () in the GRN orchestrating dorsal-ventral limb patterning.
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http://dx.doi.org/10.1186/s13227-019-0141-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842170PMC
November 2019

Sox enters the picture.

Elife 2018 10 1;7. Epub 2018 Oct 1.

Evolutionary Ecology, Department Biology II, Ludwig-Maximilians Universität München, Martinsried, Germany.

The discovery of a gene that regulates two segmentation mechanisms in spider embryos is fueling the ongoing debate about the evolution of this crucial developmental process.
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http://dx.doi.org/10.7554/eLife.41136DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6167050PMC
October 2018

Homeobox Gene Duplication and Divergence in Arachnids.

Mol Biol Evol 2018 09;35(9):2240-2253

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
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http://dx.doi.org/10.1093/molbev/msy125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107062PMC
September 2018

Expression and function of the zinc finger transcription factor Sp6-9 in the spider Parasteatoda tepidariorum.

Dev Genes Evol 2017 11 7;227(6):389-400. Epub 2017 Nov 7.

Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, Georg-August-Universität Göttingen, 37077, Göttingen, Germany.

Zinc finger transcription factors of the Sp6-9 group are evolutionarily conserved in all metazoans and have important functions in, e.g., limb formation and heart development. The function of Sp6-9-related genes has been studied in a number of vertebrates and invertebrates, but data from chelicerates (spiders and allies) was lacking so far. We have isolated the ortholog of Sp6-9 from the common house spider Parasteatoda tepidariorum and the cellar spider Pholcus phalangioides. We show that the Sp6-9 gene in these spider species is expressed in the developing appendages thus suggesting a conserved role in limb formation. Indeed, RNAi with Sp6-9 in P. tepidariorum leads not only to strong limb defects, but also to the loss of body segments and head defects in more strongly affected animals. Together with a new expression domain in the early embryo, these data suggest that Sp6-9 has a dual role P. tepidariorum. The early role in head and body segment formation is not known from other arthropods, but the role in limb formation is evolutionarily highly conserved.
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http://dx.doi.org/10.1007/s00427-017-0595-2DOI Listing
November 2017

The house spider genome reveals an ancient whole-genome duplication during arachnid evolution.

BMC Biol 2017 07 31;15(1):62. Epub 2017 Jul 31.

Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Background: The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum.

Results: We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication.

Conclusions: Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.
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http://dx.doi.org/10.1186/s12915-017-0399-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5535294PMC
July 2017

Rapid diversification of homothorax expression patterns after gene duplication in spiders.

BMC Evol Biol 2017 07 14;17(1):168. Epub 2017 Jul 14.

Abteilung für Entwicklungsbiologie, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Georg-August-Universität, Göttingen, Germany.

Background: Gene duplications provide genetic material for the evolution of new morphological and physiological features. One copy can preserve the original gene functions while the second copy may evolve new functions (neofunctionalisation). Gene duplications may thus provide new genes involved in evolutionary novelties.

Results: We have studied the duplicated homeobox gene homothorax (hth) in the spider species Parasteatoda tepidariorum and Pholcus phalangioides and have compared these data with previously published data from additional spider species. We show that the expression pattern of hth1 is highly conserved among spiders, consistent with the notion that this gene copy preserves the original hth functions. By contrast, hth2 has a markedly different expression profile especially in the prosomal appendages. The pattern in the pedipalps and legs consists of several segmental rings, suggesting a possible role of hth2 in limb joint development. Intriguingly, however, the hth2 pattern is much less conserved between the species than hth1 and shows a species specific pattern in each species investigated so far.

Conclusions: We hypothesise that the hth2 gene has gained a new patterning function after gene duplication, but has then undergone a second phase of diversification of its new role in the spider clade. The evolution of hth2 may thus provide an interesting example for a duplicated gene that has not only contributed to genetic diversity through neofunctionalisation, but beyond that has been able to escape evolutionary conservation after neofunctionalisation thus forming the basis for further genetic diversification.
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http://dx.doi.org/10.1186/s12862-017-1013-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513375PMC
July 2017

Observations on germ band development in the cellar spider Pholcus phalangioides.

Dev Genes Evol 2016 11 1;226(6):413-422. Epub 2016 Sep 1.

Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Georg-August-Universität Göttingen, Abteilung für Entwicklungsbiologie, 37077, Göttingen, Germany.

Most recent studies of spider embryonic development have focused on representatives of the species-rich group of entelegyne spiders (over 80 % of all extant species). Embryogenesis in the smaller spider groups, however, is less well studied. Here, we describe the development of the germ band in the spider species Pholcus phalangioides, a representative of the haplogyne spiders that are phylogenetically the sister group of the entelegyne spiders. We show that the transition from radially symmetric embryonic anlage to the bilaterally symmetric germ band involves the accumulation of cells in the centre of the embryonic anlage (primary thickening). These cells then disperse all across the embryonic anlage. A secondary thickening of cells then appears in the centre of the embryonic anlage, and this thickening expands and forms the segment addition zone. We also confirm that the major part of the opisthosoma initially develops as a tube shaped structure, and its segments are then sequentially folded down on the yolk during inversion. This special mode of opisthosoma formation has not been reported for entelegyne spiders, but a more comprehensive sampling of this diverse group is necessary to decide whether this peculiarity is indeed lacking in the entelegyne spiders.
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http://dx.doi.org/10.1007/s00427-016-0562-3DOI Listing
November 2016

Neofunctionalization of a Duplicate dachshund Gene Underlies the Evolution of a Novel Leg Segment in Arachnids.

Mol Biol Evol 2016 Jan 6;33(1):109-21. Epub 2015 Oct 6.

Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Georg-August-Universität, Göttingen, Germany

The acquisition of a novel function, or neofunctionalization, protects duplicated genes from redundancy and subsequent loss, and is a major force that drives adaptive evolution. Neofunctionalization has been inferred for many duplicated genes based on differences in regulation between the parental gene and its duplicate. However, only few studies actually link the new function of a duplicated gene to a novel morphological or physiological character of the organism. Here we show that the duplication of dachshund (dac) in arachnids (spiders and allies) is linked with the evolution of a novel leg segment, the patella. We have studied dac genes in two distantly related spider species, the entelegyne spider Parasteatoda tepidariorum and the haplogyne spider Pholcus phalangioides. Both species possess two paralogous dac genes that duplicated before the split between entelegyne and haplogyne spiders. In contrast to the evolutionarily highly conserved dac1, its duplicate dac2 is strongly expressed in the patella leg segment during embryogenesis in both species. Using parental RNA interference in P. tepidariorum we show that dac2 is required for the development of the patella segment. If dac2 function is impaired, then the patella is fused with the tibia into a single leg segment. Thus, removing the function of dac2 experimentally reverts P. tepidariorum leg morphology into a stage before the duplication of dac and the evolution of the patella segment. Our results indicate that the origin of the patella is the result of the duplication and subsequent neofunctionalization of dac in the arachnid lineage.
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http://dx.doi.org/10.1093/molbev/msv200DOI Listing
January 2016

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox gene labial.

Proc Biol Sci 2015 Sep;282(1814)

The intercalary segment is a limbless version of the tritocerebral segment and is present in the head of all insects, whereas other extant arthropods have retained limbs on their tritocerebral segment (e.g. the pedipalp limbs in spiders). The evolutionary origin of limb loss on the intercalary segment has puzzled zoologists for over a century. Here we show that an intercalary segment-like phenotype can be created in spiders by interfering with the function of the Hox gene labial. This links the origin of the intercalary segment to a functional change in labial. We show that in the spider Parasteatoda tepidariorum the labial gene has two functions: one function in head tissue maintenance that is conserved between spiders and insects, and a second function in pedipalp limb promotion and specification, which is only present in spiders. These results imply that labial was originally crucial for limb formation on the tritocerebral segment, but that it has lost this particular subfunction in the insect ancestor, resulting in limb loss on the intercalary segment. Such loss of a subfunction is away to avoid adverse pleiotropic effects normally associated with mutations in developmental genes, and may thus be a common mechanism to accelerate regressive evolution.
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http://dx.doi.org/10.1098/rspb.2015.1162DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4571697PMC
September 2015

Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum.

Evodevo 2015 28;6:15. Epub 2015 Apr 28.

Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Georg-August-Universität Göttingen, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany.

Background: Two visual systems are present in most arthropod groups: median and lateral eyes. Most of our current knowledge about the developmental and molecular mechanisms involved in eye formation in arthropods comes from research in the model system Drosophila melanogaster. Here, a core set of retinal determination genes, namely, sine-oculis (so), eyes absent (eya), dachshund (dac), and the two pax6 orthologues eyeless (ey) and twin of eyeless (toy) govern early retinal development. By contrast, not much is known about the development of the up-to-eight eyes present in spiders. Therefore, we analyzed the embryonic expression of core retinal determination genes in the common house spider Parasteatoda tepidariorum.

Results: We show that the anlagen of the median and lateral eyes in P. tepidariorum originate from different regions of the non-neurogenic ectoderm in the embryonic head. The median eyes are specified as two individual anlagen in an anterior median position in the developing head and subsequently move to their final position following extensive morphogenetic movements of the non-neurogenic ectoderm. The lateral eyes develop from a more lateral position. Intriguingly, they are specified as a unique field of cells that splits into the three individual lateral eyes during late embryonic development. Using gene expression analyses, we identified a unique combination of determination gene expression in the anlagen of the lateral and median eyes, respectively.

Conclusions: This study of retinal determination genes in the common house spider P. tepidariorum represents the first comprehensive analysis of the well-known retinal determination genes in arthropods outside insects. The development of the individual lateral eyes via the subdivision of one single eye primordium might be the vestige of a larger composite eye anlage, and thus supports the notion that the composite eye is the plesiomorphic state of the lateral eyes in arthropods. The molecular distinction of the two visual systems is similar to the one described for compound eyes and ocelli in Drosophila, suggesting that a unique core determination network for median and lateral eyes, respectively, might have been in place already in the last common ancestor of spiders and insects.
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http://dx.doi.org/10.1186/s13227-015-0011-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4450840PMC
June 2015

Divergent role of the Hox gene Antennapedia in spiders is responsible for the convergent evolution of abdominal limb repression.

Proc Natl Acad Sci U S A 2012 Mar 15;109(13):4921-6. Epub 2012 Mar 15.

Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Georg-August-Universität Göttingen, 37077 Göttingen, Germany.

Evolution often results in morphologically similar solutions in different organisms, a phenomenon known as convergence. However, there is little knowledge of the processes that lead to convergence at the genetic level. The genes of the Hox cluster control morphology in animals. They may also be central to the convergence of morphological traits, but whether morphological similarities also require similar changes in Hox gene function is disputed. In arthropods, body subdivision into a region with locomotory appendages ("thorax") and a region with reduced appendages ("abdomen") has evolved convergently in several groups, e.g., spiders and insects. In insects, legs develop in the expression domain of the Hox gene Antennapedia (Antp), whereas the Hox genes Ultrabithorax (Ubx) and abdominal-A mediate leg repression in the abdomen. Here, we show that, unlike Antp in insects, the Antp gene in the spider Achaearanea tepidariorum represses legs in the first segment of the abdomen (opisthosoma), and that Antp and Ubx are redundant in the following segment. The down-regulation of Antp in A. tepidariorum leads to a striking 10-legged phenotype. We present evidence from ectopic expression of the spider Antp gene in Drosophila embryos and imaginal tissue that this unique function of Antp is not due to changes in the Antp protein, but likely due to divergent evolution of cofactors, Hox collaborators or target genes in spiders and flies. Our results illustrate an interesting example of convergent evolution of abdominal leg repression in arthropods by altering the role of distinct Hox genes at different levels of their action.
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http://dx.doi.org/10.1073/pnas.1116421109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3323954PMC
March 2012

Novel function of Distal-less as a gap gene during spider segmentation.

PLoS Genet 2011 Oct 20;7(10):e1002342. Epub 2011 Oct 20.

Georg-August-Universität Göttingen, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, GZMB Ernst-Caspari-Haus, Göttingen, Germany.

Despite many aspects of the regulation of segmentation being conserved among arthropods, the evolution of novel gene functions has played an important role in the evolution of developmental regulation and the emergence of new segmental structures. Moreover the study of such novel gene functions can be informative with respect to the patterns and direction of evolutionary changes in developmental programs. The homeobox gene Distal-less (Dll) is known for its conserved function in appendage development in metazoans. In arthropods, Dll is required for the specification of distal appendage structures. Here we describe a novel and unexpected role of Dll in the spider Achaearanea tepidariorum. We detect At-Dll transcripts not only in the appendages, but unexpectedly also in an anterior domain during early development, prior to the specification of the limb primordia. A similar early Dll domain is present in the distantly related spider Pholcus phalangioides. In A. tepidariorum this early At-Dll expression is required for head segmentation. RNA interference results in spiders that lack either the first or the first and the second walking leg segments. The early At-Dll expression is also required for the activation of the segment polarity genes engrailed and hedgehog in this region. Our work identifies the Distal-less gene as a novel factor in anterior spider segmentation with a gap gene-like function. This novel role of Dll is interesting because Dll expression is reduced in this region in crustaceans and the homologous insect segment, the mandible segment, does not express Dll and does not require this gene for patterning. We therefore discuss the possible implications of our results for understanding the evolution and diversification of the mandible segment.
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http://dx.doi.org/10.1371/journal.pgen.1002342DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3197691PMC
October 2011