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An analysis of segmentation dynamics throughout embryogenesis in the centipede Strigamia maritima.

ABSTRACT: Most segmented animals add segments sequentially as the animal grows. In vertebrates, segment patterning depends on oscillations of gene expression coordinated as travelling waves in the posterior, unsegmented mesoderm. Recently, waves of segmentation gene expression have been clearly documented in insects. However, it remains unclear whether cyclic gene activity is widespread across arthropods, and possibly ancestral among segmented animals. Previous studies have suggested that a segmentation oscillator may exist in Strigamia, an arthropod only distantly related to insects, but further evidence is needed to document this.Using the genes even skipped and Delta as representative of genes involved in segment patterning in insects and in vertebrates, respectively, we have carried out a detailed analysis of the spatio-temporal dynamics of gene expression throughout the process of segment patterning in Strigamia. We show that a segmentation clock is involved in segment formation: most segments are generated by cycles of dynamic gene activity that generate a pattern of double segment periodicity, which is only later resolved to the definitive single segment pattern. However, not all segments are generated by this process. The most posterior segments are added individually from a localized sub-terminal area of the embryo, without prior pair-rule patterning.Our data suggest that dynamic patterning of gene expression may be widespread among the arthropods, but that a single network of segmentation genes can generate either oscillatory behavior at pair-rule periodicity or direct single segment patterning, at different stages of embryogenesis.

SUBMITTER: Brena C

PROVIDER: S-EPMC3879059 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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An analysis of segmentation dynamics throughout embryogenesis in the centipede Strigamia maritima.

Brena Carlo C Akam Michael M

BMC biology 20131129

<h4>Background</h4>Most segmented animals add segments sequentially as the animal grows. In vertebrates, segment patterning depends on oscillations of gene expression coordinated as travelling waves in the posterior, unsegmented mesoderm. Recently, waves of segmentation gene expression have been clearly documented in insects. However, it remains unclear whether cyclic gene activity is widespread across arthropods, and possibly ancestral among segmented animals. Previous studies have suggested th ...[more]

PMID: 24289308

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Project description:Strigamia maritima (Myriapoda; Chilopoda) is a species from the soil-living order of geophilomorph centipedes. The Geophilomorpha is the most speciose order of centipedes with over a 1000 species described. They are notable for their large number of appendage bearing segments and are being used as a laboratory model to study the embryological process of segmentation within the myriapods. Using a scaffold derived from the recently published genome of Strigamia maritima that contained multiple mitochondrial protein-coding genes, here we report the complete mitochondrial genome of Strigamia, the first from any geophilomorph centipede. The mitochondrial genome of S. maritima is a circular molecule of 14,938 base pairs, within which we could identify the typical mitochondrial genome complement of 13 protein-coding genes and 2 ribosomal RNA genes. Sequences resembling 16 of the 22 transfer RNA genes typical of metazoan mitochondrial genomes could be identified, many of which have clear deviations from the standard 'cloverleaf' secondary structures of tRNA. Phylogenetic trees derived from the concatenated alignment of protein-coding genes of S. maritima and >50 other metazoans were unable to resolve the Myriapoda as monophyletic, but did support a monophyletic group of chilopods: Strigamia was resolved as the sister group of the scolopendromorph Scolopocryptos sp. and these two (Geophilomorpha and Scolopendromorpha), along with the Lithobiomorpha, formed a monophyletic group the Pleurostigmomorpha. Gene order within the S. maritima mitochondrial genome is unique compared to any other arthropod or metazoan mitochondrial genome to which it has been compared. The highly unusual organisation of the mitochondrial genome of Strigamia maritima is in striking contrast with the conservatively evolving nuclear genome: sampling of more members of this order of centipedes will be required to see whether this unusual organization is typical of the Geophilomorpha or results from a more recent reorganisation in the lineage leading to Strigamia.

Project description:Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history.

Project description:BACKGROUND:There have been few studies of head patterning in non-insect arthropods, and even in the insects, much is not yet understood. In the fly Drosophila three head gap genes, orthodenticle (otd), buttonhead (btd) and empty spiracles (ems) are essential for patterning the head. However, they do not act through the same pair-rule genes that pattern the trunk from the mandibular segment backwards. Instead they act through the downstream factors collier (col) and cap'n'collar (cnc), and presumably other unknown factors. In the beetle Tribolium, these same gap and downstream genes are also expressed during early head development, but in more restricted domains, and some of them have been shown to be of minor functional importance. In the spider Parasteatoda tepidariorum, hedgehog (hh) and otd have been shown to play an important role in head segmentation. RESULTS:We have investigated the expression dynamics of otx (otd), SP5/btd, ems, and the downstream factors col, cnc and hh during early head development of the centipede Strigamia maritima. Our results reveal the process of head condensation and show that the anteroposterior sequence of specific gene expression is conserved with that in insects. SP5/btd and otx genes are expressed prior to and during head field formation, whereas ems is not expressed until after the initial formation of the head field, in an emerging gap between SP5/btd and otx expression. Furthermore, we observe an early domain of Strigamia hh expression in the head field that splits to produce segmental stripes in the ocular, antennal and intercalary segments. CONCLUSIONS:The dynamics of early gene expression in the centipede show considerable similarity with that in the beetle, both showing more localised expression of head gap genes than occurs in the fly. This suggests that the broad overlapping domains of head gap genes observed in Drosophila are derived in this lineage. We also suggest that the splitting of the early hh segmental stripes may reflect an ancestral and conserved process in arthropod head patterning. A remarkably similar stripe splitting process has been described in a spider, and in the Drosophila head hh expression starts from a broad domain that transforms into three stripes.

Dataset Information

An analysis of segmentation dynamics throughout embryogenesis in the centipede Strigamia maritima.

Publications

An analysis of segmentation dynamics throughout embryogenesis in the centipede Strigamia maritima.

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